Anatomy, Evolution, and Functional Significance Of

Home , Asiatosuchus, Brachychampsa, Canine penis, Countercurrent exchange, Dorsal nasal artery, Kevin Padian

ANATOMY, EVOLUTION, AND FUNCTIONAL SIGNIFICANCE OF

CEPHALIC VASCULATURE IN ARCHOSAURIA

A dissertation presented to

the faculty of

the College of Arts and Sciences of Ohio University

In partial fulfillment

of the requirements for the degree

Doctor of Philosophy

Jayc Clinton Sedlmayr

June 2002 This dissertation entitled

ANATOMY, EVOLUTION, AND FUNCTIONAL SIGNIFICANCE OF

CEPHALIC VASCULATURE IN ARCHOSAURIA

JAYC CLINTON SEDLMAYR

has been approved for

the Department of Biological Sciences

and the College of Arts and Sciences by

Lawrence M. Witmer

Associate Professor of Anatomy

Leslie A. Fleming

Dean, College of Arts and Sciences Sedlmayr, Jayc Clinton PhD. June 2002. Biological Sciences

Anatomy, Evolution, and Functional Significance of Cephalic Vasculature in Archosauria

(398 pp.)

Director of Dissertation: Lawrence M. Witmer

Cephalic vasculature is an integral component of the vertebrate head, having a major effect on morphological organization, physiological processes, and various mechanical functions

(e.g., erectile tissues). It is thus surprising that so little is known about cephalic vasculature in Archosauria, a major amniote clade that today includes crocodilians and birds and in the past included non-avian dinosaurs, pterosaurs, and a variety of basal forms. No comparative studies exist on archosaur head vasculature and no previous attempt has been made to determine homologous structures and patterns across Archosauria. Better understanding of archosaur head vasculature is key to interpreting and reconstructing the evolution of heads and head vasculature in amniotes. This study addresses this problem by documenting and comparing cephalic vascular structures and patterns in the extant archosaur clades

Crocodylia (Alligator mississippiensis, Crocodylus spp.) and Aves (Anas platyrhynchos, Struthio) and makes hypotheses of homology based on similarity. Data were attained from a variety of techniques including vascular injection, gross dissection, production of vascular corrosion casts, and the development of a novel stereoangiographic technique. Emphasis is given to the relationships of vessels to other soft-tissue structures and the bony skull, and causal associations between vascular structures and their osteological correlates are identified.

These findings are discussed in light of the radical morphological changes that occur in birds

(e.g., brain enlargement) and crocodilians (e.g., basicranial metamorphosis) to produce their highly apomorphic head anatomies that considerably deviate from the ancestral condition and were hypothesized to significantly effect and alter head vasculature in extant archosaurs.

The striking conclusion of the research is that despite their different cephalic morphologies, the vascular structures and patterns in Aves and Crocodylia are very similar. In several areas these vascular structures had clear osteological correlates shared by the two clades, and that are identifiable in fossil archosaurs. Crocodilians and birds share several, interconnected, potential vascular physiological devices that would allow for brain temperature regulation.

This interconnected network may further serve as a transport system for products produced in the Harderian gland and retina to the brain.

Approved by Lawrence M. Witmer

Associate Professor of Anatomy 5

DEDICATION

To my ancestors—for my existence and their genes and their epigenetic influences.

Especially Harriet Plattner, Fred and Ilene Sedlmayr whose nurturance, dedication, and skill in rearing is largely responsible for the man who produced this document. For all the trips to natural history museums and zoos, and for all the books and instruction on Life that my

family provided and encouraged.

To my educators and instructors who whetted and satiated my insatiable curiosity and who

provided and facilitated the knowledge required to produce this dissertation.

Suzanne Hiltz, Valerie Hinchliff, Dudley Weiland, Bonnie Harden,

Joe Domko, Elaine Anderson,

James Hanken, Alan De Quieroz, Richard Stuckey,

Bryan Small, Audrone Biknevicus, and Lawrence Witmer stand out.

To my wife Melissa Sedlmayr for Being.

To the memories of Charles Robert Darwin

and George Gordon, Lord Byron

for perspective, inspiration, and guidance through my dalliances in all things biological.

ACKNOWLEDGMENTS

Very special thanks to my committee members Audrone Biknevicus (Ohio University),

Robert Carr (Ohio University), Stephen M. Reilly (Ohio University), John Wible (Carnegie

Museum of Natural History), and Lawrence Witmer (Ohio University). I had great admiration for John Wible’s research long before becoming a graduate student. My early perusals of John’s work deeply inspired my interest, and love, for the blood vascular system and its evolution. John Wible has significantly contributed to our understanding of mammalian blood vasculature, and my original intent upon embarking on this study was to make a similar contribution to our knowledge of archosaurian blood vasculature—although a seemingly impossible task, I can only hope that this dissertation comes close to meeting my goal. It is for all these reason that I am honored to have had John serve on my committee.

The original draft of this dissertation presented to John was in parts unseemly, and John’s role as a fount of anatomical knowledge was extended to that of proofreader and editor to which I am forever grateful. Robert Carr contributed a significant amount of time and effort to this manuscript. As one of the more erudite vertebrate anatomists I have had the pleasure to know, Bob has been a constant source of anatomical information and a bewildering array of ideas and insights. Stephen Reilly has been a strong advocate of graduate research during my stay at Ohio University and an enthusiastic supporter of this dissertation. In fact, Steve’s passionate interest in evolutionary morphology was a frequent source of inspiration. Audrone Biknevicus frequently provided me with advice and assistance that was critical in getting me through this process. Audrone further served as 7 one of my gross anatomy instructors, and it was from Audrone that I truly learned head

anatomy (in considerable detail). Just as important, Audrone was always available to provide

emotional assistance. Finally, to my advisor Lawrence Witmer, who labored intensely on

this manuscript and who taught me everything from numerous lab techniques to scientific illustration. Most importantly, Larry taught me how to conduct scientific research. I had the great fortune of apprenticing under one of today’s greatest anatomists. Larry’s perspective on comparative anatomy permeates the entirety of this dissertation. I thank Robert Henry

(College of Veterinary Medicine, University of Tennessee) and Kevin Zippel (National

Amphibian Conservation Center, Detroit Zoological Society) for initial instruction in vascular injection techniques, and Tim Ganey (Atlanta Medical Center) and Julian Baumel

(Burke Museum, Seattle) for sharing their expertise in radiopaque vascular injection media and methods. Joseph Eastman and Audrone Biknevicius (Ohio University) provided access to x-ray facilities. Robert Hikida (Ohio University) provided helpful advice and training in a wide array of anatomical approaches. Scott Moody (Ohio University) provided specimens and helpful discussion. Special thanks to Ruth Elsey and The Rockefeller Wildlife Refuge,

Grand Chenier, Louisiana for providing Alligator specimens. Kent Vliet (University of

Florida) and the St. Augustine Alligator Farm, St. Augustine, Florida, provided Alligator and

Crocodylus specimens. For access to specimens, thanks to: Kevin Padian, Pat Holroyd, and

John Hutchinson, University of California Museum of Paleontology, UC Berkeley; Angela

Milner, Sandra Chapman, and David Gower, Natural History Museum of London; Rupert

Wild, Staatliches Museum für Naturkunde, Stuttgart; Michael Maisch, University of

Tübingen; Dino Frey, Staatliches Museum für Naturkunde, Karlsruhe; Johann Welman,

National Museum, Bloemfontein, South Africa; Mike Raath and Bruce Rubidge, Bernard 8 Price Institute of Paleontology, Johannesburg; Heidi Fourie, Transvaal Museum, Pretoria;

Anusuya Chinsamy-Turan, Derek Ohland, and Sheena Kaal, South African Museum, Cape

Town. Clay Corbin (Ohio University) provided invaluable advice on statistical approaches and also reviewed the first chapter. Thanks to Scott Sampson (University of Utah), John

Ruben (Oregon State University), Willem Hillenius (College of Charleston), Casey Holliday

(Ohio University), Andrew Clifford (Ohio University), Sue Simon (Ohio University), Sue

Rehorek (Slippery Rock University of Pennsylvania), Debbie Wharton (Universtity of

Bristol), Pat O’ Conner (Ohio University), Bryan Small (Denver Museum of Nature and

Science), and Michael Papp for additional productive discussion and assistance. Dana Zurn,

Stephanie Strange, and Anne Stewart provided financial support and assistance. Ryan

Ridgely (Ohio University), Andrew Lammers (Ohio University), and Melissa Sedlmayr helped with tables and illustration. I could never have completed (or survived) this dissertation without my wife, Melissa. Funding was provided by Ohio University

(Departments of Biological Sciences and of Biomedical Sciences), and the National Science

Foundation (IBN-9601174 and IBN-0076421). 9

TABLE OF CONTENTS Dedication ...... 5 Acknowledgments...... 6 Table of Contents...... 9 List of Tables ...... 15 List of Figures...... 16 List of Figures...... 16 Abbreviations...... 18 Chapter 1 A Rapid Technique for Imaging the Blood Vascular System Using Stereoangiography...... 21 Introduction...... 21 Materials and Methods...... 23 Study Taxon ...... 23 Injection Medium...... 23 Instrumentation...... 24 Experimental Procedures...... 24 Stereoradiography ...... 25 Evaluation of Injection Media...... 26 Results ...... 27 Injection Media...... 27 Stereoradiography ...... 30 Discussion...... 31 Chapter 2 Cephalic Vasculature in Extant Archosauria I: Basal Aves, With Special Emphasis on Anas Platyrhynchos and Struthio Camelus...... 34 Introduction...... 34 Previous Research ...... 36 Birds in Phylogenetic and Historical Context...... 40 Organization of Paper ...... 42 Materials and Methods...... 43 Taxa Studied...... 43 Vascular Injection...... 44 Stereoangiography ...... 45 Vascular Corrosion Casting...... 45 Gross Dissection...... 46 Results ...... 47 Proximal Vascular Branching and the Craniocervical Musculature...... 47 Vagus Artery...... 49 Pharyngeal Artery ...... 49 Origin of the Internal Carotid Artery ...... 50 Occipital Artery...... 50 Occipital Artery and its Branches in Ratites...... 52 Endocranium and the Cerebral carotid artery...... 55 Cranial Carotid Canal and the Internal Carotid Artery...... 56 Sphenopalatine and Sphenomaxillary Arteries...... 56 10 Encephalic Vasculature in Extant Aves...... 58 Encephalic Venous System ...... 58 Ethmoid Veins and the Dorsal Sagittal Sinus...... 58 Sphenotemporal Sinus...... 60 Torcular Herophili and its Tributaries ...... 62 The Trigeminal Vein—Rostral Semicircular Vein System...... 63 Trigeminal Vein ...... 63 Rostral Petrosal Sinus ...... 64 Rostral Semicircular Vein ...... 65 Caudal Petrosal Sinus...... 66 Basilar Sinuses...... 70 The Accessory Nerve and the Dural Venous Sinuses ...... 71 Endolymphatic Sac ...... 74 Cerebellar Auricular Fossa and Sinuses ...... 74 Cavernous Sinus...... 77 Basicranial Fenestra and Notocordal Crest...... 79 Encephalic Arterial System ...... 81 Caudal Encephalic Artery ...... 85 Basilar Artery ...... 86 Caudoventral Cerebellar Artery ...... 86 Tympanic and Temporal Regions...... 89 Stapedial Artery...... 89 Acoustic Artery ...... 90 Temporoorbital Artery...... 91 Dorsal Aspect of the Temporal Fossa and the Profundotemporal Artery ...... 94 Profundus Artery...... 95 Ophthalmic Rete ...... 96 Lateral Aspect of the Temporal Space...... 98 Ventral Course of the Temporal Artery...... 98 Postorbital Plexus...... 101 Trigeminal Artery...... 102 Orbital Region ...... 102 Myology and Osteology of the Orbit ...... 102 Harderian Gland ...... 107 Venous Drainage and Arterial Supply of the Eye and Eye Musculature ...... 107 Dorsal Ramus of the Ophthalmotemporal Vein ...... 107 Ophthalmotemporal Vein ...... 108 Ophthalmic Vein ...... 110 Orbital Branches of the Stapedial Artery...... 113 Supraorbital Artery...... 113 The Bony Orbital Margin...... 113 Nasal Gland...... 115 Ophthalmotemporal Artery...... 116 The Lacrimal and Nasal Gland Nerves...... 119 Orbital Artery...... 119 Palpebral Artery ...... 119 11 Hyolaryngeal Structures and the Laryngopharynx ...... 120 Caudal Hyoidal Artery ...... 120 Oromandibular Trunk...... 121 Esophagotracheal Artery ...... 121 Descending Esophageal Artery ...... 121 Descending Tracheal Artery...... 122 Hyolingual Artery ...... 122 Sublingual Artery...... 123 Proper Lingual Artery...... 124 Infraorbital and Antorbital Space ...... 125 Temporomandibular Trunk ...... 125 Rostral Auricular Artery...... 125 Common Maxillomandibular Artery...... 126 Mandibular Artery ...... 126 Jugal Artery...... 127 Pterygoid Artery...... 130 Palatomaxillary and Dorsal Alveolar Arteries...... 133 Brief survey of the Infraorbital, Antorbital, and Palatal Vasculature in Ratites ...... 136 Oropharynx...... 140 Basic Anatomy of the Caudal Oropharynx...... 140 Sphenopalatine Artery...... 142 Submandibular Artery...... 145 Rictal Artery...... 145 Median Palatine Artery ...... 146 Palatine Nerve and Artery...... 151 Nasal Cavity ...... 153 Anatomy and Vasculature of the Nasal Vestibule ...... 155 Brief Overview of the Cephalic Venous System ...... 162 Discussion...... 167 The Apomorphic Avian Head...... 167 Unique Traits in Bird Skulls...... 167 Orbit ...... 173 Modification of Facial Anatomy...... 174 Vascular Physiological Devices and Brain Temperature Regulation...... 174 Evidence for Brain Cooling...... 175 Ophthalmic Rete ...... 179 Vascular Physiological Devices Other than the Ophthalmic Rete ...... 180 Interconnected Network of Vascular Physiological Devices and the Brain ...... 182 Suborbital Plexus...... 185 Nasal Vestibular Vascular Plexus and Narial Erectile Tissue...... 187 Vessels of the Nasal Vestibular Vascular Plexus...... 197 Chapter 3 Cephalic Vasculature in Archosauria II: Crocodylia, With Special Reference to Alligator Mississippiensis...... 201 Introduction ...... 201 Biological Importance of Head Vasculature ...... 203 12 Previous Research ...... 204 Organization of the Paper...... 205 Materials and Methods...... 205 Taxa Studied...... 205 Vascular Injection...... 207 Vascular Corrosion Casting...... 208 Gross Dissection...... 210 Results ...... 210 Proximal Branching and the Craniocervical Musculature...... 210 Common Carotid Artery and the Hypapophyseal Canal...... 210 External Carotid Artery ...... 212 Occipital Artery...... 212 Proper External Carotid Artery...... 214 Internal Carotid Artery...... 214 Sphenoid Artery...... 217 Encephalic Vasculature of Extant Crocodylia ...... 218 Major Osteological Correlates of Encephalic Vascular Structures...... 218 Tentorial Crest...... 218 Osteological Correlates of the Rostral Petrosal Sinus and External Occipital Vein ...... 219 Cerebellar Auricular Fossa and Sinus...... 221 Metotic Fissure ...... 222 Encephalic Arterial System ...... 222 Encephalic Venous Sinuses...... 227 Ventral and Dorsal Sagittal Sinuses...... 227 Sphenotemporal Sinus...... 228 Torcular Herophili ...... 229 Rostral Petrosal Sinus...... 230 Formation of the Rostral Petrosal Sinus...... 230 Internal Trigeminal Foramen...... 231 Course of the Rostral Petrosal Sinus ...... 231 External Occipital Vein ...... 233 Cavernous Sinus...... 233 Spinal Accessory Nerve...... 234 Endolymphatic Sac ...... 237 Vagal Sinus...... 238 Basilar Sinus...... 239 Metotic Sinus ...... 241 Brief Survey of Cephalic Venous Drainage ...... 241 Tympanic and Temporal Regions...... 242 Stapedial Artery and Canal ...... 242 Auricular Artery and Plexus...... 244 Cranioquadrate Canal...... 244 Anatomy of the Postorbital Region...... 245 Osteology of the Temporal Canal...... 248 Vasculature of the Dorsal Temporal Fossa ...... 250 13 The Lateral Temporoorbital Artery and Vein...... 250 Medial Temporoorbital Artery and Vein...... 252 Lateral Postorbital Canal and Plexus ...... 252 Vasculature of the Temporal Canal and the Temporal Rete...... 255 Orbital Region ...... 256 Myology and Osteology of the Orbit ...... 256 Lacrimal Gland...... 258 Orbital Vasculature...... 258 Supraorbital Artery and Vein...... 259 Ophthalmotemporal Artery and Vein...... 261 The Ocular Plexiform Ring ...... 264 Orbital Artery ...... 266 Harderian Gland ...... 267 Rostral Ramus of the Trigeminal Artery...... 267 Palatine Ramus of the Facial Nerve...... 271

Ventral Division of the Dorsal Ramus of CN VIIp ...... 271 Dorsal Division of the Dorsal Ramus of CN VIIp ...... 275 Lateral Temporal Space and Mandible...... 275 Osteology and Myology of the Lateral Temporal Space ...... 275 Lateral Ramus of the Trigeminal Artery...... 277 Temporal Artery ...... 279 Trigeminal Vein ...... 280 Temporomandibular Artery...... 281 Pterygoid Artery...... 282 Maxillomandibular Artery...... 283 Mandibular Artery ...... 283 Ventral Branches of the Mandibular Nerve...... 285 Maxillary Artery...... 287 Palatomaxillary Artery...... 288 Facial Artery ...... 289 Rostral Auricular Artery...... 290 Infraorbital Space...... 291 Contributions to the Palatine Artery...... 293 Palate and Palatine Artery...... 295 Oromandibular Trunk...... 296 Buccopharyngeal Cavity...... 298 Surface Anatomy of the Region of the Choanae and Rostrodorsal Pharynx ...... 298 Mucosa and Relationships of the Laryngophayrnx ...... 301 Hyolingual Artery ...... 302 Laryngeal Artery...... 305 Nasal Cavity ...... 310 Olfactory Tract and Vasculature ...... 310 Medial Nasal Artery...... 313 Lateral Nasal Artery and Vein ...... 314 Narial Erectile Tissue and the Nostril ...... 318 Dorsal Alveolar Artery...... 319 14 Facial Vascular Plexus and the Narial Erectile Tissue...... 322 Discussion...... 323 The Apomorphic Crocodilian Head...... 323 Stapedial System...... 326 (1) External Occipital Artery...... 327 (2) External Occipital Vein ...... 327 (3) Cerebral Ophthalmic Artery ...... 328 (4) Sphenoid Artery...... 332 Palatine Vasculature, Gaping Behavior, and Gular Flutter...... 334 Elements of the Circumpharyngeal Ring ...... 336 Cephalic Vasculature and the Epiphysis-Harderian Gland-Hypothalamus Axis...... 339 Biological Importance of Melatonin...... 341 Innervation of the Harderian Gland Blood Vessels...... 343 Functions of the Harderian Gland...... 346 Literature cited...... 350

LIST OF TABLES

Table 1. Synonymy and skeletal attachments of craniocervical musculature (based on Sedlmayr and Holliday, in prep.)...... 371 Table 2. Synonymy and skull attachments of archosaur jaw adductor musculature (Holliday and Sedlmayr, in prep.). *Rows of attachments divided into crocodilians on top and birds on bottom...... 374 Table 3. Osteological correlates of encephalic vessels...... 377 Table 4. Osteological correlates of the stapedial arterial system...... 378 16 LIST OF FIGURES

Figure 1. Stereoangiographs of parasagittally sectioned domestic duck head (Anas platyrhynchos; OUVC 9441) injected with a medium consisting of 45% barium and 55% latex, and demonstrating a lateral perspective (A) and a medial perspective (B). In (B), the same stereoangiographs have been swapped (left for right), accounting for the reversed perspective. In (A) the eye and scleral ossicles (bony eye ring) stand out as superficial structures, and the tongue appears deep to the mandible. The common carotid artery is a large vessel coursing rostrally from the neck, dorsal to the trachea. The palatine artery is a median vessel running along the palatal vault; given that the head has been sectioned, the palatine artery appears as a deep structure in (A) and a superficial structure in (B). The premaxillary artery originates from the rostral aspect of the premaxilla, appearing superficial in (A) and deep in (B). The rhamphothecal artery is a small caliber vessel that arises midway along the palatine artery, traveling laterally toward the observer in (A) and away from the observer in (B). Note that despite the exact same information content, the different perspectives in (A) and (B) impart a tangibly different anatomical emphasis. Note that the 45% barium medium highlights physiologically important vascular devices, such as vascular plexuses and erectile tissues in the nasal conchae, along the pterygoid, and the ophthalmic rete caudoventral to the eye. Abbreviations: car a, common carotid artery; mand, mandible; nas con, nasal conchae; pal a, palatine artery; pmax a, premaxillary artery; rham a, rhamphothecal artery; scl os, scleral ossicles; ton, tongue...... 379 Figure 2. Scatter plots of densitometer value versus the percent of barium in the injection medium for (A) common carotid, (B) palatine, (C) rhamphothecal, and (D) premaxillary arteries for nineteen duck heads injected with a barium/latex solution varying in 5% increments. Densitometer values are unit-less and are based on a scale of increasingly more darkly shaded bars numbered 1 to 21, with 1 being most radiodense (white; densitometer value of 0.0) and 21 most radiolucent (black; densitometer value of 3.24). Thus, the closer a reading is to 0.0, the more likely a vessel is to be visualized. The plots for the common carotid (A) and premaxillary (D) arteries illustrate an increase in vessel radiopacity with increasing barium content in the injection media; non- parametric Spearman rank correlation tests demonstrated a positively significant relationship between radiopacity and barium percentage (common carotid artery, Rho = 0.700; premaxillary artery, Rho = 0.730). The plots for the palatine (B) and rhamphothecal (C) arteries do not show statistically significant relationships (rhamphothecal artery, Rho = 0.18; palatine artery, Rho = 0.200)...... 381 Figure 3. Scatter plot illustrating the relationship between the number of vessels counted (with 20 total possible vessels) versus percent barium for 19 different vascular injection solutions. The graph illustrates a fairly constant number of observable vessels (between 16 and 19 vessels) in solutions with 20%–95% barium. However, a dramatic threshold occurs at 10% barium where the number of observable vessels decreases (four vessels at 10% barium, two vessels at 5% barium). Between 40% and 55% barium, vessel number counts decrease slightly, the result of extreme vessel profusion, as some vessels are lost from view within a dense tangle of vessels (i.e., retia and erectile tissues). The Spearman rank correlation tests did not find a significant relationship (Rho = 0.400)...... 382 17 Figure 4. Phylogenetic relationships of (A) Avemetatarsalia (topology based on Sereno 1991; Benton 1999; Merck 1997), (B) Crurotarsi (based on Sereno 1991; Parrish 1993; Gower and Walker in prep.), (C) Archosauromorpha (based on Gauthier 1986; Sereno 1991; Parrish 1993; Merck 1997)...... 383 Figure 5. Phylogenetic relationships of the extant avian taxa studied (topology after Sibley and Ahlquist 1990; Cooper et al. 2001; Cracraft 2001; Cracraft and Clarke 2001; Livezey and Zusi 2001). * denotes taxa studied by dissection...... 384 Figure 6. Anas platyrhynchos. The major cephalic arteries and their relation to the bony skull in (A) lateral; (B) Dorsal; and (C) palatal views. Skull drawings based on Komárek (1979) and specimens...... 385 Figure 7. Aquila chrysaetos. Schematic illustration of the antorbital sinus and the suborbital diverticulum during (A) jaw abduction and (B) jaw adduction. The curved arrow indicates the course of the airstream. Modified from Witmer (1995b)...... 388 Figure 8. Dendogram of the Nasal vestibular Vascular Plexus (NVVP) and its elements in extant Diapsida...... 389 Figure 9. Phylogenetic relationships of Crocodylomorpha (topology based on Benton and Clarke 1988; Poe 1997; Brochu 1999). * denotes taxa studied by dissection...... 390 Figure 10. Alligator mississippiensis. The major cephalic arteries and their relation to the bony skull in (A) right lateral, (B) dorsal, (C) palatal, and (D) occipital views. Skull drawings based on Jollie (1962) and specimens...... 391 Figure 11. Crocodylus novaeguineae. Juvenile. Medial view of right side in sagittal section depicting (A) the bony endocranium and (B) the cephalic arterial system. Rostral is toward the left of the page and dorsal toward the top...... 395 Figure 12. Diagrams of the major components and divisions of the hyobranchial musculature in (A) Aves and (B) Crocodylia, based on Edgeworth (1935). Terminology of avian muscles based on Vanden Berge and Zweers (1993). Parenthetical terms in (B) refer to term used by Schumacher (1973)...... 397

ABBREVIATIONS

acc fess accessory nerve fossa acc pt accessory nerve protuberance an ad anastomosis with dorsal alveolar artery aur ct auricular cavernous tissue aur fs auricular fossa b basilar artery cb ceratobranchiale cc common carotid artery cce caudal cerebral artery ce cerebral ethmoid artery ce fs cerebral fossa cen caudal encephalic artery cn IV trochlear nerve foramen cn VII facial nerve foramen cn XII hypoglossal nerve foramen cp choanal plexus cve caudoventral cerebellar artery da dorsal alveolar artery do deep occipital artery dr dorsal rictal artery e ethmoid artery ec external carotid artery elym d endolymphatic duct eo external occipital artery f facial artery f ex occ v foramen external occipital vein fc frontal cerebral artery ft frontal bone H Harderian artery hyl hyolingual artery hyp fs hypopophyseal fossa ic fm internal carotid foramen ih interhemispheric artery im intramandibular artery is internal carotid artery j jugal artery l lingual artery ln lateral nasal artery lp lateral palatine artery lt temporal artery m mandibular artery 19 m sn an medial subnarial anastomosis max maxillary artery mce middle cerebral artery mec fs mesencephalic fossa met fs metotic fissure mlp medial palatine artery mm maxillomandibular artery mn medial nasal artery mp median palatine artery n nasal artery n et narial erectile tissue o orbital artery oc occipital artery om oromandibular artery op ophthalmotemporal artery ot occipital artery p pterygoid artery pap palatine plexus pl proper lingual artery plpd plexus of lateral pharyngeal diverticulum plt palatine artery pm palatomaxillary artery pr profundus artery prm premaxillary artery pvvb paravestibular vascular bundle r rictus ra rostral auricular artery rce rostral cerebral artery re rostral encephalic artery rer rostral erectile artery rse rostral semicircular eminence s stapedial artery shd sphenopalatine artery shm sphenomaxillary artery sl sublingual artery sm submandibular artery so supraorbital artery socc supraoccipital tm temporomandibular artery tnt tentorial crest to temporoorbital artery trig trigeminal artery trig f trigeminal foramen v vagus artery v op ventral branch of ophthalmotemporal artery v sn ventral subnarial artery 20 va ventral alveolar artery vr ventral rictal artery

CHAPTER 1

A RAPID TECHNIQUE FOR IMAGING THE BLOOD VASCULAR SYSTEM

USING STEREOANGIOGRAPHY

Introduction

Vasculature is a difficult aspect of vertebrate anatomy to study and document. Gross

dissection and serial sectioning can be effective, providing precise three-dimensional anatomical relationships of vessels to each other and to other structures (O’Donoghue, 1921;

Midtgard, 1984). These traditional methods, however, are destructive and time consuming, and are feasible for only very small samples. Angiography, the radiography of specimens injected with radiopaque substances (i.e., contrast agents), does not destroy (consume) the specimen and is much faster, enabling preparation of larger samples. However, with traditional x-ray techniques, such as plain film radiography, angiography has the major limitation of superimposition. That is, all three-dimensional anatomy is compressed into two dimensions, such that in, for example, a lateral radiograph, left and right structures are superimposed. Thus, there can be great difficulty in determining three-dimensional position

(e.g., is a vessel medial or lateral, dorsal or ventral?) and the relationships of vessels to other structures (e.g., medial or lateral to a bone, through or external to musculature, supplying the brain or the scalp). As a result, the time efficiency of angiography comes at the expense of anatomical detail and clarity. Additionally, typical radiopaque injection media offer no advantages for subsequent dissection or sectioning in that they have such low viscosity that they essentially “bleed out” of the specimen during subsequent preparation. 22 We present here a new angiographic technique that meets the need for: (1) the

elimination of superimpositioning problems; (2) subsequent dissectibility; (3) high vascular

perfusion; (4) high radiopacity; and (5) a time- and cost-efficient means of generating a large

sample size to assess variation.

There are at least four popular vascular injection media used in comparative

anatomy. (1) Liquid latex is an excellent medium for dissection studies, offering high

perfusion and excellent strength. However, latex is not radiopaque. (2) unsaturated poliester

resin (e.g., Batson’s No.17, Polysciences, Inc., Warrington, PA) is excellent for the

production of vascular corrosion casts (e.g., Tompsett, 1970), but is not radiopaque, and its

brittleness makes it unsuitable for dissection. (3) Microfil (Flow Tek, Inc., Boulder, CO), a low-viscosity silicone rubber, is a radiopaque substance and sets into a solid, making it both dissectible and well suited for radiography. Microfil, however, is relatively very expensive, has only moderate radiopacity, and has a short shelf life, after which radiopacity declines. (4)

Iodinated contrast agents are commonly used in clinical angiography, and are safe and have high perfusion. However, such media are expensive and offer no ability for subsequent dissection. We have experimented with all four media.

Our technique consists of two novel elements: (1) a new vascular injection medium

that combines the best attributes of the media just discussed; and (2) the introduction of

stereoradiography as the principle means of visualizing and analyzing angiographic data. The

new vascular injection medium is a mixture of a barium sulfate suspension and latex. Latex

is both a carrier and stabilizer for the liquid barium, which otherwise is highly viscous, less

likely to penetrate small caliber vessels, and will not “set up.” Ganey et al. (1990) introduced

the use of a barium enema solution to study vessels radiographically, but used gelatin as the 23 carrier and stabilizer. We found this medium to be much less effective than the one proposed here in terms of subsequent dissectibility. Moreover, preparation of the medium has additional steps and hence is more time consuming.

Stereoradiography, and its variant here, stereoangiography, are radiographic applications of stereoscopic imaging, a well understood means of restoring three dimensionality by viewing a pair of two-dimensional images taken from different angles with a stereoscope. Stereoradiography is an under-appreciated anatomical tool (Smith and Smith,

1967), and has seen only limited use in clinical and industrial settings (Kumazaki, 1991).

Materials and Methods

Study Taxon Heads of thirty domestic duck, Anas platyrhynchos, comprised the sample and were obtained from a commercial processor (Joe Jurgielewicz and Son Ltd., Shartlesville, PA).

Twenty heads were used in statistical analyses concerning the effectiveness of differing barium to latex ratios. Ten heads were used as replicates, and for more specialized techniques. All specimens and radiographs have been accessioned into the Ohio University

Vertebrate Collections (OUVC), and the data are available upon request from LMW.

Injection Medium The vascular injection medium tested here consisted of a mixture of barium and latex. Again, barium is the radiologic contrast agent, and latex stabilizes the barium and allows subsequent dissection of the specimen. For the barium component, we used Liquid

Polibar Plus barium sulfate suspension (BaSO4; E-Z-Em, Inc., Westbury, NY) which was developed for visualization of the gastrointestinal tract via rectal administration (barium 24 enema). For the latex component, we used a laboratory grade latex (Ward’s, Rochester, NY)

specifically designed for vascular injection.

Instrumentation The injection apparatus consisted of 18 gauge Hamilton blunt-ended cannulae

(Hamilton Company, Reno, NV) and B-D syringes with Luer-Lok tips (Becton Dickinson

and Co., Franklin Lakes, NJ). Ethicon (Cincinnati, OH) 4-0 silk suture was sometimes used to ligate cannulated vessels. A Hewlett Packard Faxitron Series 43805N Cabinet X-Ray

System was the x-ray source. The x-rays were shot on Kodak (Rochester, NY) Industrex M

Professional x-ray film and processed with Kodak Developer GBX and Kodak Rapid Fixer.

Density readings of selected vascular structures were obtained by using a densitometer (X-

Rite Company, Grandville, MI). Stereoscopes included a 4X pocket stereoscope (Alan

Gordon, Hollywood, CA) for smaller images and a Geoscope mirror stereoscope for larger images.

Experimental Procedures All injections were performed via both common carotid arteries, approximately

midway along the neck. An opening was made by making a cut ¼ to ¾ across the artery. A

blunt-ended cannula was inserted, and the needle was subsequently pushed as far cranially as

possible. In some cases, suture material was used to hold the cannula in place, but with

vessels of the size of duck common carotids, it was found that this could be accomplished

more simply and cost effectively with hemostats.

Twenty different 60 ml solutions consisting of different barium to latex ratios were

prepared, starting with a mixture of 95% barium and 5% latex and decreasing in barium

content in increments of 5% to end at a final solution of 100% latex. Large particles of latex 25 that might obstruct the injection apparatus were filtered out with fine mesh cheese-cloth.

The filtered latex was then drawn into syringes and added to the barium, which previously had been measured into a beaker. The solution was then mixed for three minutes, after which it was drawn into syringes and completely injected into a duck head through the in- place cannulae. All injected heads were immediately frozen or refrigerated overnight to allow the medium to set

Ganey et al. (1990) heated a barium sulfate and gelatin mixture to 57ºC before injection. To test the effectiveness of a heated solution versus an unheated solution, eight duck heads were injected with a barium/latex solution, four heated to 57º and four at room temperature.

Stereoradiography Plain film x-rays of the duck heads were produced using standard techniques. All duck heads were exposed in lateral view, except for a few specifically prepared for dorsoventral radiographs. As mentioned, stereoradiography requires making two slightly different x-rays of each subject, and two methods have been proposed in the literature

(Zangerl and Schultze, 1989). The first involves moving the x-ray tube, whereas the second involves moving the specimen. The latter was employed here. Heads were placed on a thin

Plexiglas square, which was then set on a section of film, with the remaining film blocked off with lead sheets to protect from exposure. The Plexiglas was then tilted by placing a 14 mm block just under its edge, taking care that the block did not overlap the specimen. The head was then exposed for 15 minutes at 30 kVp and 2.5 mA. The block was then carefully removed from beneath the Plexiglas without moving the head, and the Plexiglas was slid to an area of unexposed film. The block was then placed under the Plexiglas edge directly 26 opposite its prior location, thus tilting in the opposite direction of the prior exposure. The

head was then exposed as before.

After film development, the two images were cut out, placed on a light table beneath

a stereoscope, and aligned to attain the three-dimensional effect (Fig. 1). The opposite

perspective of the subject can be gained by interchanging the two images. For instance, the

original configuration of the two x-rays may give a lateral perspective of the head (Fig. 1A)

so that lateral features (e.g., mandible) appear closer to the observer, and medial features

(e.g., tongue) appear more distant. Swapping the x-rays, left for right (Fig. 1B), reverses the

perspective such that the observer now gains a medial view (e.g., with the tongue appearing

closer than the mandible). Although the information content of the x-rays obviously has

not changed, swapping the images and reversing the perspectives invariably leads to the

perception of a “different” anatomical emphasis.

Finally, depth resolution can be artificially enhanced by increasing tilt, which can be

useful for resolving anatomical components that are nearly in the same place.

Evaluation of Injection Media To allow statistical analysis of the effects of injection media with differing levels of barium, all specimens were x-rayed with precisely the same settings, and the films were

processed simultaneously to eliminate any error resulting from the time-sensitive nature of

chemical processing. To assess the effect of barium percentage on the radiopacity of

injected vessels, measurements were taken of the radiopacity of selected arteries using a

densitometer for each of the 20 barium percentage levels. The four arteries selected for this

analysis were (Fig. 1A): (1) the common carotid artery, which was the largest; (2) the palatine

artery; (3) a rhamphothecal artery; and (4) the premaxillary artery which is the most rostral 27 and among the smallest identifiable vessels. For each vessel at each barium percentage level,

three readings were taken and then averaged. A non-parametric statistical test, the Spearman

rank correlation, was used to test for a significant relationship between barium percentage

and radiopacity. Additionally, for each of the tests, a corresponding bivariate scatter plot

was generated to test for trends. In a second statistical study, the x-rays from the first

analysis were scored for the presence or absence of 18 large- to intermediate-sized vessels.

The total number of observed vessels was recorded for each of the 20 different solutions

and the data were analyzed using the same statistical methods.

Results

Injection Media The scatter plot of the densitometer values recorded for the common carotid artery

(Fig. 2A) indicates very little difference between treatments above a threshold at the 20% barium level, below which radiolucency steadily increases (i.e., densitometer values steadily increase) with each decrease in barium. The Spearman rank correlation test rejected the null hypothesis of no significant relationship between percent barium and the radiopacity of the common carotid artery (Rho = 0.700).

Scatter plots for the rhamphothecal (Fig. 2B) and palatine arteries (Fig. 2C) show a more variable distribution of points than was seen with the common carotid artery. The rhamphothecal and palatine arteries could not be detected below 5% and 10% barium, respectively. Subsequent dissection revealed that these radiolucent vessels were in fact completely filled by the latex/barium solutions. The Spearman rank correlation tests for both the rhamphothecal (Rho = 0.180) and palatine (Rho = 0.200) arteries accepted the null hypotheses that the radiopacity of these vessels was not dependent upon percentage of 28 barium. These analyses indicate that there is no significant difference in the radiopacity of the rhamphothecal and palatine arteries for solutions of between 15% and 95% barium.

Nevertheless, inspection of the plots (Fig. 2B-C) reveals a threshold for visualizing these vessels at about 10% barium.

The scatter plot for the premaxillary artery (Fig. 2D) indicates a linear relationship between the percentage of barium in the injection medium and the radiopacity of the injected vessel. Radiolucency of the premaxillary artery increases with decreasing barium percentage. The premaxillary artery was not observable in x-rays from solutions with 5%,

10%, and 20% barium. The Spearman rank correlation test rejected the null hypothesis, finding a significant relationship between percent barium and radiopacity (Rho = 0.730).

Analysis of the effect of barium percentage on the number of vessels observable in x-ray demonstrates a similar pattern to that found for the effect of barium percentage on radiopacity. The scatter plot (Fig. 3) indicates very little difference in the vessel counts for solutions with barium percentages between 15% and 95%. At both 15% and 95% barium,

17 out of 18 designated arteries could be identified in x-ray. A dramatic decrease in vessel count occurs at the level of 10% barium with only four of the 18 vessels observable, and at

5% barium with only three observable vessels. The Spearman rank correlation test for effect of barium percentage on the number of observable vessels for the 15% – 95% barium range accepted the null hypothesis (Rho = 0.400).

The scatter plot nevertheless demonstrates a slight decrease in the number of vessels observable in the midrange levels (40%–55% barium). Inspection of the x-rays from all of the solutions showed that the midrange barium percentages had filled a large number of small vessels associated with the conchal and pharyngeal arterial plexuses such that large- 29 and intermediate-sized arteries passing through or near these dense vascular structures are no

longer identifiable as independent structures (Fig. 1B). Thus, the loss of vessel resolution

with barium percentages between 40% and 55% can be attributed to an increase in barium in

overfilled, small caliber vessels (i.e., these plexuses were so bright they obscured other structures). Further analysis of the x-rays revealed a drastic decline in the number of intermediate and small caliber vessels beginning with the 20% barium solution. The conchal and pharyngeal plexuses are no longer detectable in the 20% and lower barium solutions.

The same phenomenon was observed for the dense array of vessels associated with the jaw and cervical musculature.

Analyses of the number of observable vessels and their radiopacity demonstrate a

threshold at 15% to 20% barium, below which resolution is severely compromised.

Furthermore, we found no significant differences in vessel counts and radiopacity of

between solutions of 25% to 95% barium. At 20% barium, many large- and intermediate-

sized vessels were visible but very faint, and resolution of small caliber vessels, including

important physiological structures such as retia and plexuses, was nearly lost. Below 20%

barium, only the largest vessels were observable, and they were so radiolucent that they too

were nearly undetectable.

The effects of heating injection medium (as done by Ganey et al., 1990) were

compared to those of room-temperature injections through a qualitative analysis of x-rays.

No discernable differences in radiopacity or perfusion could be detected. Thus, this time-

consuming step was dropped from our protocols.

Subsequent dissectibility of the injected heads represents a major advantage over

conventional angiographic techniques. Even at moderate barium concentrations, the latex 30 component of the injection medium ensured all of the dissection benefits of conventional

latex injection (e.g., rubbery toughness of the injected vessels, enhanced detectability due to

coloration of the latex). However, there is a marked decrease in the dissectibility of

specimens injected with high barium (i.e., low latex) content solutions. Vessels injected with

low latex content solutions are more delicate, easily torn, and difficult to see due to the lower

levels of pigment. An unexpected (but welcome) result was that, despite the “dilution” of

latex with liquid barium, casts of vessels sometimes survived the skeletonization process

(e.g., treatment with dermestid beetles), yielding vascular corrosion casts. Thus, the same

injected specimen could yield useful data via angiography, dissection, and corrosion casting.

Stereoradiography As predicted, stereoscopic examination eliminated the problem of superimposition.

Many vessels could only be resolved among the tangle of vessels when analyzed in stereo.

The stereoangiographs provided information concerning vessel position in three- dimensional space, the precise origin of vessels, the relationships of the vessels to other vascular structures (e.g., retia), and clarification of the tissues supplied by particular vessels.

For example, the stereoangiographs demonstrated that particular vessels supplied the brain rather than running through the scalp. None of the above information was obtainable in normal two-dimensional analysis of the x-rays. In summary, the use of stereoradiographs dramatically increased the amount of meaningful information that could be recorded. In some ways, it duplicated information that was previously only obtainable through labor- intensive gross dissection but, moreover, revealed vessels and anastomoses that dissection would have missed. 31 Discussion

Our goal was to develop a technique that would go beyond the standard

angiographic objectives of high perfusion and radiographic resolution. We also wanted to

eliminate the problem of superimposition and to allow for subsequent gross dissection.

Moreover, our intent was to develop protocols that were fast, easy, and inexpensive, so that

large samples could be surveyed. Thus, we developed an injection medium characterized by

high vascular perfusion, high radiopacity, and high dissectibility, and analyzed the resulting angiographs stereoscopically, solving the superimposition problem.

Any barium- and latex-based solution possessing between 25% and 95% barium will

produce high resolution radiographs. Solutions with extremely high barium content (e.g.,

75% or more) have highly radiopaque vessels, but suffer in two major areas: (1) diminished

perfusion of small vessels because of the large barium particle size and hence increased

viscosity; and (2) poor dissectibility, because of the concomitant reduced latex content.

Barium solutions with extremely low barium content (e.g., 25% or less) have excellent

perfusion and dissectibility (due to the high concentration of latex), but at the expense of

radiopacity to the extent that very few (if any) vessels are observable in radiographs.

Solutions approximating 50:50 barium to latex ratios are characterized by both high

perfusion and radiopacity, and can illuminate important vascular structures. They have a low

enough viscosity to allow the filling of small and far distal vessels, yet still contain enough

barium particles to produce highly radiopaque vascular structures. As a result, these

solutions provide important physiological insights by radiographically demonstrating

vascular structures such as retia and arterial plexuses that are involved in countercurrent heat

and gas exchange. These solutions further provide indications of the relative blood supply 32 to anatomical structures, such as jaw musculature used in feeding, or conchae (Fig. 1B) that are involved in protecting against heat and water loss during respiration. However, this increased filling can obscure vascular structures observable in higher or lower barium concentrations. If the extremes are avoided, a researcher can essentially “eyeball” the mixture and obtain excellent results. If the researcher is interested in gross dissection, we recommend lower barium concentrations (e.g., one-third barium, two-thirds latex).

Obviously, each solution carries its own costs and benefits and different solutions can be used to address different questions.

Stereoradiography remains a seldom used, and apparently, poorly known anatomical technique. The technique has been used and advocated for addressing paleontological questions (Zangerl, 1965), and to assess fish anatomy (Smith and Smith,

1967). Stereoangiography has been used only rarely in a clinical context, and, where it has

(e.g., Lunsford et al., 1977; Kumazaki, 1991), it is associated with high cost and

(understandably) limited anatomical scope. To our knowledge, stereoangiography has never been used in comparative anatomical studies like ours. Angiographs are notoriously difficult to decipher as a result of superimpositioning of vessels and other dense tissues such as bone.

Stereoangiographs provide powerful resolution of the three-dimensional spatial position of individual vascular structures, and the positional relationships of vascular elements to other anatomical structures. The production of stereoradiographs is a simple technique that requires little additional expenditure of time or cost. Any radiographic study of vascular systems should use stereoradiography as an integral tool.

The technique advocated here is particularly advantageous in addressing variation in vasculature within and between populations, and in comparative studies of vasculature 33 across groups of animals. For small- to medium-sized organisms, several specimens can often be exposed and analyzed on a single film. Although the documentation of the vascular system has in the past been a highly time-consuming occupation, often necessitating the recording of a system in great detail in a single specimen (or a small number of specimens), this technique can provide a new means of understanding the variation of vascular systems in natural populations.

CHAPTER 2

CEPHALIC VASCULATURE IN EXTANT ARCHOSAURIA I: BASAL AVES,

WITH SPECIAL EMPHASIS ON ANAS PLATYRHYNCHOS AND STRUTHIO

CAMELUS

Introduction

The amniote head is the intersection of the neural, sensory, respiratory, and digestive systems. The head is a center of numerous sensory systems by which an amniote receives information about its environment, and obviously, through the brain, the head serves as the center by which these and other data are processed and synthesized, and from which orders for subsequent responses are given. The hypothalamus is the control center of emotion, reproduction, and other behaviors. Head musculature serves as the mechanism by which an amniote feeds (acquires and processes food), vocalizes, and in mammals, expresses emotion. The various glands of the head are often used in immunological responses, salt balance, processing information about photoperiod and light intensity, and regulating circadian rhythms. Of course, the functions of the head go far beyond the short list given here.

It is upon the blood vascular system that all these structures and their functions depend. It is through the blood vascular system that these various tissues and tissue systems are provided with nutrients, that waste and toxic substances are removed, through which secreting hormones from the epiphysis, hypophysis, Harderian gland, etc. are transported through the body to other systems. Vasculature can further modify other tissue systems, such as bone, often producing grooves, foramina, and canals. Cephalic vasculature often 35 forms vascular physiological devices that act as countercurrent heat and/or gas exchange

centers, or performs complex tasks such as those associated with cavernous tissues. Given all these central roles (or vital functions) it comes as a surprise that much of the structure and pattern of head vasculature, is still unknown in many, if not most, amniote clades, in any significant detail. And it is in the amniote clade Archosauria, which includes birds and crocodilians, that our information is particularly deficient.

Data presented in this dissertation holds broad significance outside of archosaurian

biology. Vascular data can be used in determining the relationships between taxa. The

establishment of homologies in archosaurian vascular elements can provide characters that

can be combined with data from other amniote groups to give us a more refined

understanding of amniote systematics (especially for Archosauria). A more complete and

detailed understanding of cephalic vasculature in the clade Archosauria can further be used

in comparative studies on the evolution of vascular systems. The lack of information on

vasculature from birds and especially crocodilians is a major hindrance to our understanding

of how amniote vascular patterns are organized, which structures are nearly universal across

amniotes, and if there exists certain rules for vascular organization in amniote heads (and

how these rules and patterns affect other structures). Since vascular systems are known to

significantly effect the patterning and structure of other anatomical systems, including

pneumatic tissues (Witmer 1995a, b, 1997), knowledge of cephalic vasculature in a major

vertebrate clade can add greatly to our understanding of head evolution in vertebrates.

Another important component of this paper is the identification of osteological

correlates for cephalic vascular structures. Vessels often leave traces of their existence as

grooves, canals, and foramina. These forms of evidence can be used in an Extant 36 Phylogenetic Bracket approach (Witmer 1995a) to identify and reconstruct soft tissues in fossil archosaur species, and to further test similarity-based hypotheses of homology between birds and crocodilians through congruence. This approach has been effectively demonstrated in studies of non-vascular soft tissues in archosaurs, including pneumatic structures, muscles, nerves, glands, etc. (Witmer 1997) and nostril position (Witmer 2001).

By describing osteological correlates of vascular tissue in birds (this chapter) and crocodilians

(Chapter 3) and identifying shared osteological correlates between these two clades, this dissertation provides the foundation for an EPB study of cephalic vasculature in fossil archosaurs, which can provide important insight into the physiology and behavior of these organisms.

Previous Research In the past century, many studies attempting to comprehend the comparative anatomy and evolution of complex structures and systems have suffered under the insidious nature of paraphyly (Witmer 1997). Birds and crocodiles, as living sister groups and the only extant members of the clade Archosauria, have suffered the most from paraphyletic thinking. Very few attempts were made to see crocodiles outside of “reptiles,” and birds outside of a lone platonic ideal. Moreover, subsequent to the Herculean attempts during the late nineteenth and early twentieth centuries to accurately describe in gross detail the anatomies of a multitude of amniotes, to determine evolutionary patterns, and to establish

“bauplans,” many anatomical systems became subject to disinterest and have been largely ignored. Whereas the nineteenth century interest in brains, cranial nerves, the autonomic system, etc. blossomed into neurobiology and later became subjects of their own subdisciplines, the study of vasculature as a system, and as a subject of comparative anatomy, 37 has largely died. The aim of this paper is twofold, to add to our knowledge of the anatomy and evolution of amniote cephalic vasculature, and to present a highly detailed description of the anatomy of head vasculature in birds, a highly derived amniote clade.

A series of early studies sought a broader understanding of the anatomy and homologies of vasculature across amniotes (Hafferl 1933, Shiino 1914, Shindo 1914).

Unfortunately, as mentioned earlier, many of these studies suffered in their treatment of archosaurs. Crocodilians were usually compared to lepidosauromorphs or turtles, and were never discussed in relation to birds. Crocodilian anatomy was often seen as highly derived or enigmatic, and because of their seemingly disparate anatomy, crocodilians were frequently paid little attention or completely ignored. The fate of the analysis of birds was in many cases worse. Although birds have long been regarded as sauropsids (turtles, lepidosauromorphs, and crocodiles) or “reptiles,” they were frequently discussed with little comparative perspective. As a result, attempts to understand the four major clades of living amniotes (Mammalia, Testudinata, Lepidosauromorpha, Archosauria) often gave short shrift to the most speciose of the four clades (Archosauria).

Nevertheless, some remarkably elegant studies of head vasculature have been published on birds. However, in most (if not all) of these cases vasculature was treated in isolation, that is, with little reference to the rest of the head, outside of a few papers that discussed the relationship of vessels to bone. This is not to say that information on the blood supply to some muscles, glands, etc. does not exist, but there is no highly detailed account, for any bird, of the entire head vascular system comparable to what is known for, say, humans or dogs (Evans 1993). This paper attempts to offer such a foundation, that is, to present the adult head vasculature of birds (focusing on the domestic duck) in detail, 38 including the relationships of vessels to other tissues systems (e.g., what does the vessel pass through, around, along; what vessel(s) supply particular muscles, glands, etc.). The paper makes reference to other non-anseriforms birds, and discusses some fossil data from non- avian dinosaurs. Vascular embryology is a critical future direction, but such studies cannot be performed without reference to adult form.

The research presented here builds on the classic work of others. Hughes (1935), for example, presented an exhaustive study on development of the major head vessels in chickens, which has been a foundation for future research on vasculature in birds and other vertebrates. Julian Baumel has been a seminal figure in the study of avian cephalic vasculature. Baumel (1979, 1993) synthesized his and other workers’ research on avian vasculature in his chapter in Nomina Anatomica Avium and provided a nomenclatural foundation for this system and its components. The figures and vessel definitions in

Baumel’s papers are heavily oriented toward the domestic chicken, but do make important reference to other birds. In all of these papers, Baumel provides useful and highly detailed diagramatic depictions of the head vessels (arterio-and veinograms), but usually without reference to other tissues or a written description. In separate papers, Richards (1967, 1968) provided important descriptions of the major arteries and veins in chickens. Midtgard

(1984b) discussed the major head arteries in herring gulls, and provided detailed illustrations of the head vasculature with reference to the bony skull. The primary focus of this paper concerned the organization, blood supply, and function of the ophthalmic rete. In another important work, Midtgard (1984a) discussed in more detail below, on vascular physiological devices in the domestic duck, and again provided a detailed illustrative (but not written) description of the head vasculature in the domestic duck with reference to the bony skull. 39 Midtgard’s publications are part of a long line of papers discussing the anatomy and

physiology of the ophthalmic rete, which will be discussed below (e.g., Kilgore et al. 1973,

1976, 1979; Arad et al.1989). All of these papers, especially Midtgard (1984b) stand as

important foundations for this research and on which this paper hopes to expand.

However, in all these papers, the detailed anatomy of small vessels, the objects of vascular

supply, the relationships of vessels to other structures in space, and comparisons with other

bird groups or other amniotes is superficial or lacking. To be fair, such comparative

approaches and such specificity of detail were not the intent of these papers or the research programs that produced them. Most of the prior descriptive literature was provided to

establish a base for understanding physiological functions (the ophthalmic rete for example).

Comparative anatomy, with a phylogenetic evolutionary perspective, is a relatively new

domain. However, a recent series of publications on the vasculature in the archosaurian

nasal cavity (Witmer 1995b; Sedlmayr and Witmer 1998, 1999) have taken this approach.

In the last half century, attempts at a comparative and evolutionary understanding of

head vasculature have been limited to Mammalia. In a series of papers Bugge (1972, 1974,

1979) made an exhaustive attempt to describe the adult pattern of the major head vessels in

numerous basal mammals. Wible (1984, 1986, 1987) greatly advanced this work by studying

mammal head vasculature for the first time in a phylogenetic context and by providing

detailed embryological descriptions for the major head vessels. Later, Wible and Hopson

(1994) included data from fossil mammals to develop a deep-time historical perspective and

as a means of testing homology through congruence. Recent studies have examined head

vasculature in less inclusive mammalian clades (e.g., Wible and Zeller 1995 for Scandentia;

Geisler and Liu 1998 for Cetecea). Thus, for at least one amniote clade, Mammalia, we are 40 coming to a strong comparative evolutionary understanding of cephalic vasculature, and the

research presented here attempts to bring the clade Archosauria to a similar level.

Birds in Phylogenetic and Historical Context Sadly, birds are all that remain of the staggering biological diversity representing

Dinosauria. Figure 4A is a cladogram depicting the Dinosauria and its placement in

Avemetatarsalia. More specifically, Aves is a well nested clade within Theropoda, a clade of

terrestrial, and mainly predatory, dinosaurs (Ostrom 1976; Gauthier 1986; Padian and

Chiappe 1998; Sereno 1999; Norell et al. 2001; Prum 2002). Birds are important in that they

are the most speciose modern amniote clade, they have radiated into a vast array of

ecological niches and morphological varieties, and avian heads have evolved into a

bewildering array of forms to facilitate subtle and not so subtle changes in diet, sensory

perception, etc., including the attraction of mates through sexually selected cephalic

structures (combs, wattle, crests, etc.). Yet, only by envisioning a world in which all

mammals, except for bats, have become extinct, can we comprehend what was lost with the

extinction of non-avian dinosaurs. The closest living sister group to birds is Crocodylia, a

seemingly very different clade. Figure 4B is a cladogram depicting the phylogenetic

relationships of Crurotarsi, in which Crocodylia is deeply nested. And Archosauria is but a

clade nested within the much more inclusive clade Archosauromorpha (Figure 4C; Gauthier

1986; Sereno 1991; Parrish 1993), the sister group to Lepidosauromorpha, which is now considered by some researchers (Merck 1997) to include marine reptiles (plesiosaurs, ichthyosaurs, placodonts). Thus, Archosauromorpha rivaled, if not dwarfed, Mammalia in

diversity of form and function. Yet, the study of species within Crocodylia and Aves, and 41 comparison to other amniotes, is the only means biologists have to reconstruct and understand the anatomy and evolution of archosauromorph heads, blood vasculature, etc.

In the past decade, systematists and ornithologists have come to a far better understanding of the interrelationships and diversification of birds (Livezey and Zusi 2001;

Cracraft 2001). Today, Aves is represented by the clade Neornithes, which includes

Palaeognathae and the Neognathae. The palaeognaths include the Ratititae, which is an array of flightless ground birds such as ostriches, rheas and kiwis, and the Tinami, a clade of gallinaceous, volant birds (Sibley and Ahlquist 1990; Cooper et al. 2001; Cracraft 2001;

Cracraft and Clarke 2001; Livezey and Zusi 2001). Palaeognaths display an array of plesiomorphic characters more indicative of non-avian theropods than of other birds.

Neognaths comprise Galloanseres, which includes chickens and their kin (galliforms) and ducks and their kin (anseriforms) and their most recent common ancestor (Sibley and

Ahlquist 1990; Livezey 1997), and Neoaves, which includes all other living neognaths (Sibley and Ahlquist 1990; Cracraft 2001; Livezey and Zusi 2001). Interestingly, the basal avian clades, tinamous, galliforms (by their very nature), screamers (basal anseriforms), and basal neoavians (buttonquail, bustards, seriamas, etc.) are all morphologically similar,

“gallinaceous” birds. Phylogenetically, the basal neognath clade Galloanseres, with its diversity of gallinaceous birds and waterfowl, is situated between Palaeognathae and

Neoaves. It is then lucky that galloanserines also include the oldest domesticated birds, and have benefited from extensive research. Chickens have long been used for embryological studies, and have been extensively used to understand head development and organization

(Noden 1983, 1986). As such, not only are chickens, ducks, turkey, and geese easily attainable, but outside our own species and Mus, chickens and ducks, are potentially the best 42 understood vertebrates. Another fortunate circumstance is that many of the ultrastructural

anatomies and functions of the tissues described in this paper, including physiological

functions of some of the vascular devices, have been described in mallards (e.g., Midtgard

1984a). For these reasons, we provide a highly detailed description of the head vasculature in Anas platyrhynchos. However, reference is routinely made to geese, galliforms, and palaeognaths in cases where their anatomy differs from that of ducks. Very little has been published on the cardiovascular system of Palaeognathae, and thus the attention given here to ratites fills an important gap. Otherwise, the description of the duck will stand as a description of a basal bird.

Organization of Paper The Results section of this paper is organized in a caudal to rostral pattern. The

distal common carotid artery and its proximal branches are discussed first and the blood

supply to the distal rhamphotheca is discussed last. Within the rostral to caudal range,

vessels are discussed in reference to anatomical regions, such as the oropharynx and the

nasal cavity. For many of these regions, a brief anatomical description is given of their non-

vascular contents. Emphasis is consistently placed on anatomical interrelationships. Then,

within each anatomical region the vessels and their branches are described in detail,

including the specific structures these vessels supply (including muscles, bones, connective

tissues, etc.). The format follows arterial flow and ramification. Venous structures are

described in reference to the above arterial topology and not the direction of venous return

(the flow of which does not necessarily follow a rostral to caudal trajectory anyway).

However, reference will consistently be made to the relationship of venous structures in

relation to other veins, so the venous pattern will not be lost within the arterial tree. The 43 discussion will focus on changes in vascular structure and pattern in response to three highly

apomorphic features of extant bird heads: expansion of the brain enlargement of the eye,

and the reduction of the maxilla. The discussion will then focus on cephalic vascular

physiological devices (e.g., the narial vesibular vascular plexus) and their known, or potential,

role in brain cooling.

Materials and Methods

Taxa Studied Figure 5 is a cladogram depicting the relationships of the organisms used for and

discussed in this paper.

All of the following specimens used for this study were obtained as preserved or

fresh heads or whole animals, (1) mallard (Anas platyrhynchos), (2) greylag goose (Anser anser),

(3) wild turkey (Meleagris gallopavo), (4) chicken (Gallus gallus), (5) ruffed grouse (Bonasa

umbellus), (6) ostrich (Struthio camelus), (7) emu (Dromaius novaehollandiae), (8) tinamidae indet..

The above specimens were acquired from commercial sources, except for numbers three and

five, which were donated by Scott Moody, PhD.

The following specimens were studied from dried skulls in various museum collections: (1) crested screamer (Chauna torquata), USNM 18588 and 614549; (2) magpie goose (Anseranas semipalmata), T 9619; (3) fulvous whistling-duck (Dendrocygna bicolor); (4) trumpeter swan (Cygnus cygnus); (5) American black duck (Anas rubripes), S 16490; (6)

Australian brush-turkey (Alectura lathami), T 5008; (7) barred tinamous (Crypturellus parvirostris), T 9860; (8) common rhea (Rhea americana); (9) larger emu (Dromaius novaehollandiae). 44 Fossil skull material from the following non-ornithurine theropods was also studied,

(1) Hesperornis regalis, FMNH PA219; (2) Archaeopteryx lithographica, BMNH 37001; (3)

Deinonychus antirrhopus, MOR 747, OMNH 50268, YPM 5210, and YPM 5231; (4)

Dromiceiomimus brevitertius, CMN 12228; (5) Allosaurus fragilis, UUVP 5427 and CM 21703.

Institutional abbreviations: BMNH, Natural History Museum, London; CM, Carnegie

Museum of Natural History, Pittsburgh; CMN, Canadian Museum of Nature, Ottawa;

FMNH, Field Museum of Natural History, Chicago; MOR, Museum of the Rockies,

Montana State University, Bozeman; OMNH, Oklahoma Museum of Natural History,

Norman; USNM, United States National Museum, Washington, DC; UUVP, University of

Utah Museum of Natural History, Salt Lake City; YPM, Peabody Museum, Yale University,

New Haven.

Vascular Injection The following taxa were prepared by vascular injection: 30 ducks, 14 geese, two

ruffed grouse, one chicken, one emu, eight ostrich, one tinamou.

The injection apparatus consisted of 18 gauge Hamilton blunt-ended cannulae (Hamilton

Company, Reno, NV), and B-D syringes with Luer-Lok tips (Becton Dickinson and Co.,

Franklin Lakes, NJ). Ethicon (Cincinnati, OH) 4-0 Silk suture was sometimes used to ligate

cannulated vessels.

For all injections, dissecting scissors were used to make a ¼ to ¾ opening across the vessel, and a blunt-ended cannula was then inserted into the lumen and pushed as far cranially through the vessel as possible. The cannula was kept within the vessel by either tying ligature around or clamping with hemostats the area of the vessel containing the cannula. 45 Stereoangiography For this study 30 ducks, two geese, two turkey, one chicken, and two ostrich were studied via stereoangiography.

We developed a novel vascular injection medium for the production of stereoangiographs that consisted of a mixture of barium and latex. For the barium component, we used Liquid Polibar Plus barium sulfate suspension (E-Z-EM, Inc.,

Westbury, NY) (BaSO4)), and for the latex component (Ward’s, Rochester, NY), we used a laboratory grade latex injection solution specifically designed for vascular injection.

A Hewlett Packard Faxitron Series 43805N Cabinet X-Ray System was the x-ray source. The x-rays were shot on Kodak (Rochester, NY) Industrex M Professional x-ray film and processed with Kodak Developer GBX and Kodak Rapid Fixer.

The novel stereoangiographic method developed for this study is discussed in detail elsewhere (Chapter 1) and will not be elaborated on here.

Vascular Corrosion Casting In the course of the study, the following specimens were prepared as vascular corrosion casts: two mallards, one goose, two ruffed grouse, one emu, and two ostrich.

The purpose of the vascular corrosion cast was to produce a detailed cast of the cephalic arterial system without other soft tissues. Most casts were produced with an intact bony skull to provide context for interpretation of the vasculature and to determine osteological correlates of vascular structures. Additionally, vascular corrosion casts provided unique insight into complex vascular systems and structures, including the anatomy, composition, and anastomotic relations of vascular plexuses and retia.

Following the vascular injection protocol, both of the common carotid arteries were injected with red Batson’s no. 17 polyester resin (Polysciences, Inc., Warrington, PA). Blue 46 resin was injected into both jugular veins. After injection, the specimen was immediately placed in a cold-water bath and left for twelve hours to allow the medium to set up.

A 30-40% potassium hydroxide (KOH) aqueous solution was measured out in a beaker. The solution volume (e.g., 1000 ml for a 13.5 cm long goose head) and beaker size were selected to fully submerge and contain the specimen, respectively. The beaker containing the solution was then placed in a water bath (Fisher Tissue Prep Flotation Bath,

Model 134, Fisher Scientific Co., Pittsburgh, PA), and the solution was heated to 37º C. The specimen was then placed into the heated solution and closely monitored throughout the digestive process. Occasionally, the specimen was carefully removed from the solution using a fine mesh net or large forceps, placed upon a tray, and then mechanically prepared using a thin jet of water and fine point forceps. Mechanical preparation was used to remove muscle and other soft tissues from the bone with little damage to the vascular cast. The specimen was fully removed from the solution after a one to four hour period, dependent upon the extent of the soft tissue digestion and the preservation of the bony skull. The specimen was then rinsed in water for half an hour, and then placed in an aqueous solution of 10% hydrogen peroxide and 30% ammonia for one hour. The specimen was then rinsed in water for another half hour. After being removed from water, the specimen was set out to dry over a twelve-hour period. Forceps were used for subsequent pruning of excess vessels, and for dissection of the cast, under a light dissecting microscope (Nikon Stereoscopic

Microscope SMZ-U, Nikon Corporation, Tokyo, Japan).

Gross Dissection Five mallards, 14 geese, two turkey, one chicken, one emu, one tinamou, and eight ostrich were studied through gross dissection. 47 Several specimens were studied through the standard techniques of gross section.

Most of these specimens were further studied, through the use of a hacksaw, as sagittal

sections, a series of parasagittal sections, or a series of transverse sections. Other specimens

were studied by removal of the mandible and/or removal of the calotte.

Results

Proximal Vascular Branching and the Craniocervical Musculature All of the following descriptions are of Anas platyrhynchos unless stated otherwise.

Coursing cranially through the neck, the avian common carotid artery travels

through an osseomuscular canal, the carotid cervical canal (Baumel 1975, Baumel and

Witmer 1993, Vanden Berge and Zweers 1993; pers. obs.). The artery travels across the

ventral aspects of the cervical vertebrae, which forms the dorsal aspect of the canal, and

between the medial aspects of the paired carotid hypapophyseal processes which are

outgrowths of the mid-ventral area of the cervical vertebrae and which form the lateral aspects of the canal (Baumel and Witmer 1993). At each vertebral segment, fibers from mm. rectus capitis ventralis pars medialis sinistra and dextra insert into the ipsilateral hypapophyseal process and form part of the lateral aspect of the canal, whereas the muscle bellies of the two muscles form the ventral aspect of the canal. Additional muscle tendons from both left and right muscles travel rostroventromedially across the dorsal aspect of the arteries, and insert into a contralateral hypapophysis of a more cranial vertebral segment, which reinforces the dorsal component of the canal. Upon exiting the carotid cervical canal, each artery courses rostromedially, across the ventral aspect of m. rectus capitis ventralis pars medialis, to the ventrolateral aspect of m. rectus capitis pars lateralis. 48 The common carotid artery enters the craniocervical region traveling between mm. rectus capitis ventralis pars medialis and rectus capitis ventralis pars lateralis. The artery courses rostrolaterally along the medial aspect of the muscle belly of m. rectus capitis ventralis pars lateralis and the ventrolateral aspect of the esophagus. M. rectus capitis ventralis pars medialis is a large fleshy muscle oriented longitudinally along the craniocervical midline, with the right and left bellies closely apposed to each other (see Goodman and

Fisher 1962; Vanden Berge and Zweers 1993). Rostroventrally, the parabasisphenoid is triangular in shape, with the lateral aspects of the bone appearing as crests that are oriented rostromedially toward one another. Rostrally, as the rostrolateral aspects of the parabasisphenoid become confluent, the parabasisphenoid forms an extended tongue-like process, the rostral process of the parabasisphenoid that rests rostroventral to the ostium for the common pharyngotympanic tube and ventral to the infundibular crests. M. rectus capitis ventralis pars medialis has a fleshy insertion along the triangular basiparasphenoid region and along the rostral parabasisphenoid process. Pars lateralis is very much its own muscle body, with right and left bellies widely separated from one another by the two bellies of pars medialis; however, near the craniocervical junction, the right and left bellies send oblique components toward each other which fuse in a shared aponeurosis ventral to pars medialis. In its course between mm. rectus capitis ventralis pars lateralis and medialis, the common carotid artery passes across the dorsal aspect of the aponeurotic junction between pars lateralis dextra and sinistra. Figure 6A-C depict the major branches of the common carotid artery in relation to the bony skull. 49 Vagus Artery Far rostral to the aponeurosis between mm. rectus capitis pars dextra and sinistra,

the common carotid artery, which is still closely apposed to the medial aspect of m. rectus

capitis ventralis pars lateralis, gives off a large caudolaterally inclined vessel, the vagus artery

(Richards 1967; arteria comes n. vagi of Baumel 1993). The vagus artery passes across the

ventral aspect of m. rectus capitis ventralis pars lateralis and the dorsal aspect of the jugular

vein (Baumel 1975, 1993). The vagus nerve courses caudally along the vessel’s lateral aspect

(Assenmacher 1953). Assenmacher (1953) also described this vessel as coming off the

common carotid before the latter artery bifurcates into the internal carotid and external

carotid arteries, but terms it the descending esophageal artery. The artery is described as an

early branch of the occipital artery in Gallus (Richards 1967; Baumel 1975, 1993). In its

course, the artery gives off several branches that ramify across the ventral aspect of the m.

rectus capitis ventralis pars lateralis muscle belly. Rostral to the branching of the vagus

artery, the common carotid artery continues in its course along m. rectus capitis ventralis

pars lateralis with the more rostral aspect of the vagus nerve pressed against its lateral aspect.

Pharyngeal Artery The next artery to branch off the common carotid artery in Anas (and Gallus,

Richards 1967) is the pharyngeal artery, which appears to arise only from the left common

carotid. Baumel (1975, 1993) observed the artery branching off the ventral aspect of the

common carotid artery, proximal to the latter vessel giving off the internal carotid artery.

The vessel travels medially, along the ventral aspect of m. rectus capitis ventralis pars lateralis, and then gives off several rostral and caudal branches across the muscle bodies of

mm. rectus capitis ventralis pars medialis sinistra and dextra and caudo- and rostroventral

branches to the ventral esophagus. 50 The rostral hypoglossal nerve exits from the skull and passes through the double headed tendon of m. rectus capitis lateralis. The nerve then continues its ventromedial course, passes ventral to the vagus nerve, and then curves medially to pass ventral to the common carotid artery. Finally, the rostral hypoglossal nerve travels rostroventromedially to the esophagus, following, in part, along the lateral aspect of the common carotid artery.

Origin of the Internal Carotid Artery Subsequent to the branching of the pharyngeal artery, the common carotid artery becomes ventrally inclined and is no longer apposed to the craniocervical musculature. It then bifurcates into large medial and lateral vessels, the external and internal carotid arteries.

The internal carotid artery passes ventral to m. rectus capitis ventralis pars medialis and is located just medial to the depressor mandibulae musculature. The artery becomes dorsally inclined and travels across the m. rectus capitis ventralis pars medialis tendon, en route to the parabasal fossa. The vessel then sends off a caudomedial branch, the occipital artery

(Baumel 1993; Midtgard 1984a). According to Richards (1967) and Baumel (1975, 1993), the occipital artery branches from the external carotid artery in Gallus, rather than the internal carotid artery as described for Anas.

Occipital Artery The occipital artery travels dorsolaterally toward the cervical musculature and across the ventrolateral aspect of the tendon of m. rectus capitis ventralis pars lateralis. Proximally, the artery is crossed passes dorsally over the main trunk of the vagus nerve (as seen in Gallus;

Richards 1967), which then follows the common carotid artery. The vessel then branches into lateral and dorsal branches, the superficial and deep occipital arteries, respectively

(Baumel 1975, 1993). 51 The superficial occipital artery is caudolaterally inclined and immediately divides into caudal and lateral branches. The caudal branch courses caudomedially to the dorsolateral border of m. rectus capitis ventralis pars lateralis where it divides into medial and caudal branches. The larger, caudal branch travels caudally across the dorsal aspect of m. rectus capitis ventralis pars lateralis and across the ventral aspect of m. rectus capitis dorsalis. The medial branch courses caudomedially toward the rostroventrolateral aspect of the axis, and upon contacting bone, the vessel proceeds to travel caudally, across the ventromedial aspect of m. rectus capitis dorsalis and the ventrolateral aspect of the cervical vertebrae.

The lateral branch of the superficial occipital artery immediately bifurcates into caudal and rostral branches. The caudal branch travels caudodorsally to and supplies the ventral aspect of m. rectus capitis lateralis, and then travels caudally across the ventral aspect of the muscle. The rostral branch sends branches to the caudal and medial aspects of m. depressor mandibulae internus, and branch(es) that pass to the caudal aspect of m. depressor mandibulae externus at the caudal articular process which travel dorsally and laterally, giving several long braches across the body of the muscle.

The deep occipital artery courses dorsally across the lateral aspect of m. rectus capitis ventralis pars lateralis and then across the lateral aspect of the tendon of m. rectus capitis dorsalis to the dorsolateral border of the latter muscle. The nerve to m. rectus capitis lateralis courses caudoventrally between the tendon of m. rectus capitis dorsalis and the artery. Upon reaching the dorsolateral aspect of the tendon, the artery bifurcates into rostral and caudal branches. The rostral branch of the deep occipital artery, the descending vertebral artery, travels rostromedially across the tendon and medial to the cervical somatic plexus, toward the lateral aspect of the craniocervical joint. The artery then enters the first 52 transverse foramen (Midtgard 1984a), off the atlas vertebra, and then runs caudally through

the vertebrarterial canal and becomes confluent with the ascending vertebral artery.

According to Baumel (1975), the artery of the vertebrarterial canal enters the canal through

the third transverse foramen in Gallus, whereas Richards (1967) reports the vessel entering

the canal through the first transverse foramen for the same species.

The caudal branch of the deep occipital artery, arteria occipitalis dorsalis, travels caudodorsally along the dorsolateral border of m. rectus capitis dorsalis, passing between this muscle and the ventral aspect of m. rectus capitis lateralis, and then continues across the medial aspect of m. rectus capitis lateralis. The vessel, while medial to m. rectus capitis lateralis, travels between the muscle bodies of mm. rectus capitis dorsalis and splenius capitis. The vessel continues caudodorsally, past the dorsal border of m. rectus capitis lateralis, and between this muscle and m. splenius capitis; in this section of its course, the vessel is no longer laterally covered by m. rectus capitis lateralis. The vessel then gives off a long caudodorsal vessel to m. splenius capitis and the caudomedial aspect of m. rectus capitis lateralis. A large branch of this artery passes caudally between m. complexus and the dorsal aspect of m. rectus capitis dorsalis (m. complexus partially covers and then connects to m. rectus capitis dorsalis through an aponeurosis). Another branch dives deep to m. complexus, to pass between and supply the dorsal aspect of m. rectus capitis dorsalis and the ventral aspect of m. splenius capitis.

Occipital Artery and its Branches in Ratites The occipital artery in Struthio camelus branches laterally from the external carotid

artery (occasionally from the internal carotid artery), then courses rostrodorsolaterally across

the lateral aspect of m. rectus capitis lateralis, and then divides into rostral and caudal 53 branches. The caudal branch, the vagus artery, courses caudally across the medial aspect of the vagus nerve, the lateral aspect of m. rectus capitis lateralis, along the ventromedial aspect of m. rectus capitis dorsalis, dorsal to the jugular vein, and medial to m. collateralis colli.

The rostral branch of the occipital artery courses laterally, and then bifurcates, ventral to CN

X into rostral and caudal branches, the deep and superficial occipital arteries, respectively.

Caudal to the bifurcation, the vagus nerve travels caudomedially to the lateral aspect of the vagus artery.

The superficial occipital artery travels caudodorsally and then bifurcates into rostral and caudal branches. The caudal branch travels caudally across the lateral aspect of m. rectus ventralis pars lateralis. The rostral branch courses rostrodorsally and divides into a ventral branch that courses rostroventrally to the ventrolateral aspect of m. depressor mandibulae and into a rostral branch that courses rostrodorsally and sends off a series of vessels to the dorsolateral aspect of m. depressor mandibulae. A cervical nerve travels rostrocaudally along the superficial occipital artery and then across the dorsal aspect of the vessel’s rostral branch after which the nerve meets and connects with another nerve that travels caudodorsally across the ventral aspect of the nerve to m. depressor mandibulae. A branch of the spinal accessory nerve courses caudodorsally across the ventral aspect of the rostral arterial branches to m. depressor mandibulae and then turns caudally and travels in this direction along the dorsomedial aspect of m. collateralis colli, similar to Alligator.

The deep occipital artery courses rostrodorsally across the lateral aspect of m. rectus capitis ventralis pars lateralis to the ventrolateral aspect of the m. rectus capitis dorsalis tendon, then travels across the latter, and then bifurcates into rostral and caudal branches, the rostral and dorsal occipital arteries, respectively. Throughout this course, the artery is 54 ventral to the vagus nerve. The rostral deep occipital artery courses dorsally across the

rostrolateral aspect of the m. rectus capitis dorsalis tendon to the dorsolateral aspect of the

tendon, and then travels medially across the dorsal aspect of the tendon to its

rostrodorsomedialmost aspect, where the vessel is laterally crossed by a caudoventromedially

oriented branch of the first cervical nerve, which eventually enters the ventromedial aspect

of m. rectus lateralis. The artery then bifurcates into lateral and medial branches. The lateral

branch courses caudally across the dorsomedial aspect of m. rectus capitis dorsalis, the

ventromedial aspect of m. splenius capitis, and along the lateral aspect of the cervical vertebrae. The medial branch, the descending vertebral artery, travels caudally a short distance and enters the first (atlantal) transverse foramen into the vertebrarterial canal and then courses caudally through the canal and becomes confluent with the ascending vertebral artery.

The caudal branch of the deep occipital artery, the dorsal occipital artery, turns dorsally and travels to the dorsolateral aspect of the m. rectus capitis dorsalis tendon, then courses caudodorsally across the tendon, and then sends off a branch that runs rostromedially across the medial aspect of the muscle. The dorsal occipital artery then courses caudodorsally to the dorsal aspect of m. rectus capitis dorsalis, and then travels caudodorsally across the dorsal aspect of this muscle, the ventrolateral aspect of m. splenius capitis, and the medial aspect of m. rectus capitis lateralis. Throughout its course, the dorsal occipital artery travels with the first cervical nerve. The vessel and nerve then course past the dorsomedialmost aspect of m. rectus lateralis and both bifurcate into rostral and caudal branches. The rostral neurovascular bundle travels caudodorsomedially to and then across the dorsal aspect of m. splenius capitis toward the ventral aspect of m. complexus, and then 55 courses caudally between these two muscles, lateral to the lateral aspect of m. biventer

cervicis, and sends off a series of medially directed vessels that supply the latter muscle. The

rostral branch of the first cervical nerve sends off an array of nerves to m. complexus, m.

splenius capitis, and m. biventer cervicis. The caudal branch travels caudally across the

dorsal aspect of m. rectus capitis dorsalis, and the caudal branch of the first cervical nerve sends branches into the muscle.

Endocranium and the Cerebral carotid artery The rostral (continuing branch) of the internal carotid artery (Assenmacher 1953;

Baumel 1975, 1993; Midtgard 1984a), travels dorsally and slightly rostral. The artery lies in a

space defined by the sphenooccipital bridge dorsally, m. depressor mandibulae laterally, and

the retroarticular process ventrally. The artery first passes lateral to the tendon of m. rectus

capitis pars lateralis and is immediately crossed by a rostral branch of the vagus that

communicates with the glossopharyngeal nerve, this is the vagoglossopharyngeal connection

(Bubien-Waluszewska 1981). In its course, the internal carotid artery is tightly bound by the

vagus nerve caudally and the glossopharyngeal nerve rostrally. It continues to course

dorsally, across the lateral aspect of the basioccipital and then basisphenoid basal tubera, and

rostral to the tendon of m. rectus capitis dorsalis. The vessel then slips dorsal to the

glossopharyngeal nerve and sends off a dorsal branch, the stapedial artery, en route to the

stapedial foramen (Assenmacher 1953, Richards 1967, Baumel 1975, 1993, Midtgard 1984a).

The internal carotid artery then continues to travel toward the ostium of the cranial carotid

canal. Caudodorsolateral to this region is the muscular insertion of m. rectus capitis dorsalis. 56 Cranial Carotid Canal and the Internal Carotid Artery In Struthio, the internal carotid artery passes into the external ostium of the cranial carotid canal (Baumel and Witmer 1993), which is located in the dorsal face of the caudoventrolateral aspect of the basiparasphenoid. This component of the basiparasphenoid

is a wing-like bone that flares caudolaterally from the paraphenoid. The cranial carotid canal

is a caudolateral to rostromedial obliquely oriented osseous tube that is caudoventromedial

to the osseous lateral pharyngotympanic tube, which also runs through the

basiparasphenoid. Moreover, the canal rests within the ventral aspect of the rostral tympanic

recess, and ventral to the rostral tympanic diverticulum of the middle air sac. The rostral

extent of the cranial carotid canal opens into the lateral aspect of the hypophyseal fossa via a

foramen in the lateral aspect of the basisphenoid. Upon entering the cranial carotid canal,

the internal carotid artery travels rostromedially, toward the basisphenoid, for a short

distance.

Sphenopalatine and Sphenomaxillary Arteries The branching patterns of the palatine and sphenomaxillary rami from the internal

carotid artery and the morphology of the bony canals derived from the cranial carotid canal

that accommodate these vessels are very similar in anseriforms to the condition found in

Struthio camelus, which is described below. However, from these observations (also illustrated

in Midtgard 1984a), it is readily apparent that the palatine and sphenomaxillary rami are not

branches of a single sphenoid artery branching from the internal carotid artery. Rather, the

two former vessels are independently derived from the internal carotid artery. For these

reasons, I advocate discarding the terms palatine and sphenomaxillary rami of the sphenoid

artery (Baumel 1993) and propose the name arteria sphenomaxillaris for the latter artery. As

the name palatine artery already exists for another vessel, we advocate replacing palatine 57 ramus of the sphenoid artery with the term arteria sphenopalatina. This terminology will be used throughout the duration of the text.

In the caudolateral aspect of the rostral tympanic recess, the canal of the palatine ramus of the facial nerve enters the caudodorsolateral aspect of the cranial carotid canal, and the palatine ramus of the facial nerve enters into the cranial carotid canal to travel along the internal carotid artery. Just rostral, the internal carotid artery sends off a lateral branch, the sphenopalatine artery, that courses with the sphenopalatine branch of the palatine ramus of

CN VII through the osseous sphenopalatine canal, which is located in the dorsal face of the lateral aspect of the basiparasphenoid. The canal of the sphenopalatine artery is continuous with the cranial carotid canal, and is shaped as a tilted arc-like tube, laterally concave, that runs from a caudodorsolateral position to a rostroventrolateral position. The sphenopalatine artery curves through the canal and exits to the rostrolateral aspect of the basiparasphenoid through the caudal sphenoid foramen. The caudal sphenoid foramen opens into a fossa in the rostrolateral basiparasphenoid, just caudodorsomedial to the bony origin of the basipterygoid process.

After giving off the palatine ramus of the sphenoid artery, the internal carotid artery continues its rostromedial course toward the internal carotid foramen. Approximately midway through the cranial carotid canal, the internal carotid artery sends off a rostrolaterally oriented branch, the sphenomaxillary artery, which courses through the osseous sphenomaxillary canal. The sphenomaxillary canal comes off from the cranial carotid canal at an acute angle, and runs laterally through the basiparasphenoid. The sphenomaxillary artery courses laterally and exits the canal into the fossa in the rostrolateral basiparasphenoid via the orbital foramen. The lateralmost aspect of the sphenomaxillary 58 canal runs parallel and just rostral to the sphenopalatine canal, and for a distance is separated from the latter canal by a low ridge, creating a space, which would provide the two vessels with the potential to anastomose. The sphenopalatine artery courses across the caudoventral aspect of the basipterygoid process, and the sphenomaxillary artery travels across the dorsal aspect of the process.

In galloanserines the external ostium of the cranial carotid canal is situated in the rostral aspect of the parabasal fossa, which is actually the caudoventrolateral aspect of the basiparasphenoid. The canal then runs rostromedially through the rostral tympanic recess toward the lateral aspect of the basisphenoid, and is connected to the surrounding ventral and dorsal bone by slender bony struts.

Encephalic Vasculature in Extant Aves

Encephalic Venous System Ethmoid Veins and the Dorsal Sagittal Sinus

The olfactory bulbs rest against the rostralmost aspect of the olfactory canal and are rostrally, laterally, and ventrally surrounded by a dense venous plexus (Kaku 1959, Baumel

1993). The ventral aspect of the plexus is drained by a single median, longitudinally oriented vein, the ventral sagittal sinus, that courses caudally across the median dorsal aspect of the ossified supraseptale and across the median ventral aspect of the olfactory tract. Caudal to the olfactory tract, the sinus travels caudally across the median rostral floor of the rostral cranial fossa and between the ventromedial aspects of the two cerebral hemispheres.

The dorsal aspect of the plexus is drained by a single median, longitudinal sinus

(Baumel 1975, 1993), sinus olfactorius, that drains caudally across the dorsomedial aspects of 59 the olfactory tracts and against the roof of the short olfactory canal. Caudally, within the

endocranial cavity, the sinus becomes confluent with the rostrodorsal sagittal sinus.

The ethmoidal veins, which drain the nasal cavity, course through the olfactory

sulcus that runs across the dorsolateral aspect of the interorbital sinus (see the section on the

orbit below). Each sinus then passes out of the orbit and into the rostrolateral aspect of the

olfactory cavity through the olfactory foramen, which is located in the caudalmost aspect of

the olfactory sulcus. Upon entering the olfactory canal, the ethmoid vein travels

caudomedially across the dorsal aspect of the olfactory tract, and the contralateral veins

anastomose immediately or course caudally parallel to one another. The olfactory bulb

receives the olfactory nerve that courses rostrolaterally with the ethmoid arteries out of the

olfactory canal and into the orbit through the olfactory foramen.

In various specimens of Anas, the ethmoid veins appear to be separated within the

olfactory canal by a median longitudinal ridge that extends from the canal’s roof, and anastomose upon entering into the rostral aspect of the encephalic cavity. The roof of the canal is formed by the frontal bone. In other species (e.g., Dromaius), the ethmoid veins

appear to anastomose along the rostrodorsal aspect of the olfactory tract, within the canal.

In various other species, the olfactory sinus draining the dorsal olfactory plexus travels along

the ventral aspect of the median ridge of the olfactory canal, and anastomoses with each of

the ethmoid veins through a series of lateral branches. In some specimens, the anastomotic

relationships of these vessels in the canal essentially forms a venous plexus that spreads

across the roof of the olfactory canal and the dorsum of the olfactory tract. In all of these

patterns, the ethmoid veins eventually anastomose to form the dorsal sagittal sinus, and the 60 olfactory plexus eventually drains into the dorsal sagittal sinus by draining into the ethmoid

veins or directly into the sinus.

The dorsal sagittal sinus courses caudally, in the dorsal aspect of the falx cerebri, and

between the dorsomedial aspects of the two cerebral hemispheres (Richards 1967; Baumel

1975, 1993). The sinus typically travels across a median longitudinal ridge extending ventrally from the endocranial roof, formed from the frontal and parietal. This crest is formed by a partial ossification of the falx cerebri, and can be poorly developed, as in many ratite specimens, whereas the crest is typically well developed in adult Anas. In juvenile specimens, the falx cerebri is unossified, and a longitudinal groove extends across the median surface of the roof of fossa cranii rostralis. The groove is formed by the dorsal sagittal sinus, and is often present in the rostral aspect of fossa cranii rostralis in Struthio. In a few Struthio specimens, the weak sagittal ridge is cleaved into two ridges by the sinus, and a groove rests between them.

Throughout its course, the dorsal sagittal sinus receives a series of veins that drain

medially across the dorsal aspects of the cerebrum, or dorsomedially across the lateral

aspects of the cerebrum. The sinus terminates by draining into the torcular herophili.

Sphenotemporal Sinus

Rostrally, the tentorial crest is formed by a thick bony ridge projecting medially from the laterosphenoid, which is covered by a thickened dura. The tentorial crest begins on the median aspect of the laterosphenoid along the bone’s dorsal margin just ventral to the frontal-laterosphenoid suture, and extends caudally across the parietal and just dorsal to the squamosal. In birds, the tentorial crest divides fossa cranii rostralis from fossa cranii media.

The canal for the communicating ramus between the ophthalmic rete and the 61 sphenotemporal sinus opens up as a caudally facing foramen in the tentorial crest at the

juncture of the squamosal, frontal, laterosphenoid, and parietal bones. In some specimens,

the bony tentorial ridge terminates at the level of the foramen and the crest continues as

thickened dural tissue. In either case, the tentorial crest continues caudodorsally, forming

the roof of the rostral semicircular canal and then becomes confluent with the protuberantia tentorialis (Elzanowski and Galton 1991). The protuberantia tentorialis is a robust ridge that extends rostroventrally to caudodorsally across the caudomedial aspect of the parietal and forms the caudodorsal border of fossa cranii rostralis.

The sphenotemporal sinus begins on the rostroventral aspect of the cerebrum and

courses across the dorsolateral aspect of the tentorial crest, running along and draining the

ventrolateral aspect of the cerebrum and the rostrodorsal aspect of the optic tectum (Kaku

1959; Baumel 1975, 1993). In ducks, the postorbital process is formed laterally by the

squamosal and medially by the laterosphenoid bones, with a very small contribution from

the frontal bone rostrodorsomedially. A ventral foramen on the postorbital process, lateral

to crista zygomaticas in the caudal aspect of the coronoideous fossa transmits a venous

branch from the ophthalmic rete into a caudally directed canal that opens along the tentorial

crest. After exiting the canal, the vein continues caudally and drains directly into the

sphenotemporal sinus. Just caudal to this foramen, the sphenotemporal sinus splits into

dorsal and ventral branches. As mentioned above, the ventral sphenotemporal sinus passes

over the medial aspect of the tentorial crest and ultimately anastomoses with the rostral

petrosal sinus at the entrance of the rostral semicircular vein canal where it forms the rostral

semicircular vein. The dorsal branch of the sphenotemporal sinus, the transverse sinus,

continues to run on the dorsal aspect of the tentorial ridge across the parietal and drains the 62 caudoventral cerebrum and rostrolateral cerebellum. The transverse sinus then curves

caudodorsally to the protuberantia tentorialis, draining the caudolateral cerebrum, and then

drains into the torcular herophili dorsally.

Torcular Herophili and its Tributaries

The torcular herophili is a large venous sinus situated in the caudodorsolateral aspect of the lateral wall of the rostral cranial fossa and against the parietal that receives a series of veins that drain from and across the dorsolateral aspect of the cerebrum (see Wharton 2000;

Wharton and Sedlmayr 2000 for fossil archosaurs). Upon receiving these tributaries, the sinus then courses dorsomedially across the parietal as it curves to form part of the endocranial roof. In its course, the sinus curves to course caudomedially toward the dorsolateral aspect of the protuberantia tentorialis and then drains into the dorsolateral aspect of the transverse sinus. As these two sinuses intersect, they receive a third sinus that drains along the roof of the endocranium and the dorsolateral aspect of the cerebrum.

At the dorsalmost aspect of the lateral endocranial wall, the protuberantia tentorialis curves dorsomedially along the curvature of the parietal as it forms the lateral aspect of the endocranial roof. The crest then extends medially across the endocranial roof until it meets and becomes confluent with the contralateral crest, and together the crests form a single horizontal crest that runs across the mid-ventral aspect of the parietal, termed the marginal crest. In several groups (e.g., Anas), each side of the marginal crest is rostromedially oriented rather than completely horizontal and together form a V-shaped crest. When well developed, the rostral face of the crest forms a sloped, caudoventrolaterally oriented border for the caudodorsal aspect of the rostral cranial fossa. Similarly, the caudal face of the fossa forms a rostroventrally oriented slope, with a shallow fossa within it, that forms the rostral 63 border of the fossa cranii caudalis. The median, rostrodorsal aspect of the crest intersects with the rostrodorsal sagittal crest.

The transverse sinus courses rostromedially across the ventral aspect of the marginal crest, and along the median aspect of this ridge the sinus becomes confluent with the contralateral transverse sinus. The dorsal sagittal sinus drains into the median rostral aspect of the intersection of the transverse sinuses. Together, this intersection of sinuses forms the torcular herophili. Moreover, the large epiphyseal venous sinus that drains dorsally along the epiphysis empties into the ventral aspect of the torcular herophili. The torcular herophili and its lateral extensions, the transverse sinuses, expand and rests across the wide rostral slope of the marginal crest. The torcular herophili drains caudally into the narrow rostral aspect of the occipital sinus. The latter sinus courses across the median dorsal aspect of the cerebellum.

The Trigeminal Vein—Rostral Semicircular Vein System

Trigeminal Vein In Anas and Anser the trigeminal vein appears as a sinus-like structure surrounding the maxillomandibular trigeminal nerves in their course through the maxillomandibular trigeminal canal. The vein wraps around the lateral, dorsal, and ventral aspects of the nerve.

The trigeminal vein primarily drains veins associated with the medial aspect of the ophthalmic rete from the caudal orbit. The veins in the caudal aspect of the orbit drain across the m. pseudotemporalis process, flowing ventrally toward the maxillomandibular foramen along the deep aspect of m. pseudotemporalis. Additionally, the trigeminal veins receives veins draining from the pharyngeal plexus, which flow dorsally toward the maxillomandibular foramen, in a course caudal to m. protactor quadratis et pterygoidei and deep to the otic process of the quadrate. The latter two sets of veins drain into the ventral 64 aspect of the trigeminal vein. Similarly, in Gallus the trigeminal vein occupies the dorsal,

ventral, and lateral aspects of the maxillomandibular foramen. In Gallus, the profundal vein

drains through the profundal foramen and flows caudally and then laterally to empty into

the trigeminal vein.

Rostral Petrosal Sinus In Anas, a thick wall of connective tissue covers the roof of the maxillomandibular trigeminal foramen and connects to a very thick string of tissue that divides the surface of the foramen into dorsal and lateral compartments. The rostral petrosal sinus begins in the area of the dorsal, tissue-covered surface of the maxillomandibular foramen, draining blood

from, and essentially becoming a continuation of, the trigeminal vein. The sinus travels

caudodorsally, forming an osseous groove in its course on the rostromedial wall of the otic

capsule, running against the rostral margin of the rostral semicircular eminence until reaching the tentorial crest. In Anser, an ossified crest runs from the mid-dorsal maxillomandibular foramen and curves caudodorsally to the caudal extent of the tentorial crest, forming a raised bony rostral margin of the rostral petrosal sinus. In geese and some duck specimens, the caudal extent of the tentorial crest is ossified and courses caudodorsally over the rostrodorsal aspect of the rostral semicircular eminence. In this region the rostral semicircular eminence and the tentorial crest are separated by a small space creating the rostroventral aspect of the rostral semicircular vein canal through which the rostral petrosal sinus passes. In those Anas specimens with an unossified tentorial crest, the rostral petrosal sinus passes ventral to the dura of the tentorial crest to reach the dorsal semilunar groove of the rostral petrosal sinus.

Veins that drain the periorbital plexus and other orbital structures and that travel with the maxillary and mandibular trigeminal nerves through the maxillomandibular foramen are the first to drain into the origin of the rostral petrosal sinus. The venous sinus then drains and 65 runs along the caudoventrolateral aspect of the mesencephalon, and the rostrodorsal aspect

of the rhombencephalon (Kaku 1959; Baumel 1975, 1993) and then curves across the caudal

aspect of the mesencephalon. Near the entrance of the rostral semicircular vein canal, the rostral petrosal sinus anastomoses with the ventral branch of the tentorial sinus to form the rostral semicircular vein.

Rostral Semicircular Vein The rostral semicircular vein canal is medially and partially dorsally covered by a dural sleeve that is continuous with the dural lining of the tentorial crest. In some Anser specimens, the tentorial crest extends far caudally in a position just above the dorsal aspect of the rostral semicircular eminence, forming the roof of the rostral semicircular vein canal, and becomes confluent with the rostroventral aspect of the protuberantia tentorialis

(Elzanowski and Galton 1991). In all domestic duck and goose specimens, the dorsal aspect of the rostral semicircular vein canal is deeply grooved by the rostral semicircular vein, forming the floor of the canal. In these specimens, various portions of the dura lining the medial aspect of the rostral semicircular vein canal becomes ossified, occasionally appearing as either outgrowths of the rostral semicircular eminence or the tentorial crest, and often completely enclosing the rostral semicircular vein in an osseous canal. In many geese, and protuberantia tentorialis, which is bridged by a thickened dura that serves as the roof of a fibrocartilaginous rostral semicircular vein canal.

In ratites, a sinus courses caudodorsally across the medial aspect of the protuberantia tentorialis, and between the caudolateralmost aspect of the cerebrum and the rostrolateralmost aspect of the cerebellum. Ventrally, this sinus drains into the rostral semicircular vein at the intersection of the protuberantia tentorialis with the canal of the rostral semicircular vein and just dorsal to the dorsalmost aspect of the rostral semicircular 66 eminence. Dorsally, the sinus drains into the ventrolateralmost aspect of the confluence of sinuses.

Upon exiting its canal, the rostral semicircular vein is termed the external occipital vein. The external occipital vein passes caudoventrally through a groove in the rostrodorsomedial aspect of the supraoccipital, ventral to the parietal-supraoccipital suture, and exits the endocranium through a foramen in the caudodorsolateral aspect of the supraoccipital.

Caudal Petrosal Sinus Another venous sinus, the caudal petrosal sinus, drains into the caudoventrolateralmost aspect of the torcular herophili, caudoventrally across the caudal aspect of the protuberantia tentorialis. Along the mid-caudal aspect of the crest, the sinus courses caudoventrally away from the protuberantia tentorialis. Proximally, the caudal petrosal sinus receives a large sinus branch that courses caudodorsally along the parietal bone and the rostrolateral aspect of the cerebellum, and then turns and travels dorsally across the parietal toward the ventrolateral aspect of endocranial roof, and, upon reaching the roof, the sinus turns medially to course across the parietal component of the endocranial roof and the mid-dorsal aspect of the cerebellum before draining into the occipital sinus near the median aspect of the roof. The caudal petrosal sinus then courses caudoventrally across the endocranial aspect of the parietal toward the dorsal aspect of the rostral semicircular vein canal, and sends off a ventral vein that courses ventrally to anastomose with the rostral semicircular vein. The caudal petrosal sinus then curves and travels caudally across the ventromedial aspect of the parietal and the lateral aspect of the cerebellum, in a course that is dorsal and parallel to the rostral semicircular vein canal. Along its course, the caudal petrosal sinus receives a series of long veins that travel dorsolaterally from a more ventrolateral 67 aspect of the cerebellum in a position dorsal to the cerebellar auricle, and that then course across the medial aspects of the rostral semicircular and then rostral semicircular vein canal before draining into the caudal petrosal sinus.

Further caudally, the caudal petrosal sinus courses caudoventrally toward the internal aspect of the external occipital foramen, and upon reaching the caudoventromedial aspect of the parietal, the sinus bifurcates into dorsal and ventral branches. The ventral branch travels to the internal dorsal aspect of the external occipital vein foramen and then anastomoses with the caudal aspect of the rostral semicircular vein as the latter vessel exits the endocranium through the foramen and becomes the external occipital vein.

The dorsal branch of the caudal petrosal sinus travels caudodorsally along the medial aspect of the parietal-supraoccipital suture, then curves dorsomedially across the dorsolateral aspect of the suture and of the cerebellum. In ratites and galloanserines, the supraoccipital protrudes as a slender ridge along the length of the supraoccipital-parietal suture. The caudal aspect of the caudal petrosal sinus travels across the medial aspect of the marginal crest.

Dorsally, the marginal crest curves medially as the lateral wall of the endocranium becomes medially inflected to form the endocranial roof. Along the lateral aspect of the endocranial roof, the suture and its associated marginal crest become rostromedially inflected. The caudal petrosal sinus then runs rostromedially across the endocranial roof toward the interparietal suture along the median aspect of the roof, and then terminates by draining into the lateral aspect of the occipital sinus near the caudal median aspect of the endocranial roof and the caudodorsal medial aspect of the cerebellum.

The confluence between the occipital sinus and the caudal petrosal sinus at the endocranial median aspect of the parietal-supraoccipital suture forms a second confluence of 68 sinuses. This caudal confluence of sinuses has apparently received little attention from

previous workers. The rostral petrosal sinus drains the cerebellar auricle, the caudal and

ventral aspects of the mesencephalon, much of the cerebellum and the rhombencephalon,

and receives blood draining from the temporal space and the orbit, including vessels draining from the ophthalmic rete. As mentioned above, the blood of the rostral petrosal sinus drains out of the endocranium and into the jugular system via the external occipital vein.

The caudal petrosal sinus acts as a large anastomotic connection between the drainage

system of the rostral petrosal sinus and the occipital sinus, and the latter vessel swells into a

larger sinus upon reception of the caudal petrosal sinus. Additionally, the occipital sinus

rests against the cerebellum and the temperature of the sinus would be partially determined

by the blood flowing into it from the rostral petrosal sinus system, which could have

important implications for whole brain cooling (see discussion).

Caudal to the intersection of the occipital sinus and the caudal petrosal sinus is a

deep fossa, the cerebellar fossa, in the caudal aspect of the supraoccipital that is laterally

bordered by the marginal crests. As the occipital sinus courses caudally to the dorsomedial

aspect of the supraoccipital, the sinus immediately expands out laterally across the

supraoccipital and ends at the caudolateral border of the rostral semicircular eminence. The

occipital sinus fills the wide cerebellar fossa in the supraoccipital and lies across the

caudodorsal aspect of the cerebellum. In this area, the occipital sinus receives a large vein

and then drains caudodorsally from a series of vessels along the lateral aspect of the medulla

oblongata and then travels across the lateral aspect of the cerebellum. Ventrally, the

cerebellar fossa is continuous with a narrower, yet much deeper, fossa in the median

endocranial surface of the supraoccipital, which externally forms the ventral and more 69 protuberant component of a median and vertical crest extending from the the supraoccipital.

Moreover, the dorsal aspect of this crest is on the opposite side of, and potentially formed by, the more shallow and dorsal median fossa in the endocranial aspect of the supraoccipital.

The occipital sinus largely drains into this more ventral fossa, fills the fossa, and rests along the median caudoventral aspect of the cerebellum (Kaku 1959; Richards 1967; Baumel 1975,

1993). The more rostroventral aspect of the occipital sinus, within the ventral aspect of the cerebellar fossa, drains ventrally across the supraoccipital. At this point, the sinus rests against the caudoventralmost aspect of the cerebellum and the mid-caudodorsalmost aspect of the medulla oblongata. The sinus then curves and travels caudally between the foramen magnum and the spinal cord, and becomes confluent with the vertebral venous sinus, which travels caudally along the dorsal aspect of the vertebral canal and the dorsal and dorsolateral aspects of the spinal cord.

As in ratites and perhaps birds generally, the dorsal sagittal sinus of phasianids expands to form an enlarged occipital sinus, which expands to fill a vertically oriented fossa within the endocranial mid-caudal aspect of the supraoccipital, and which is rostrolaterally bordered by the caudolateral aspect of the rostral semicircular eminence. Further ventral, the occipital sinus in phasianids becomes wider by expanding further laterally across the deeper caudoventral aspect of the otic capsule along the caudal aspects of the cerebellum.

The sinus then courses caudally along the roof of the foramen magnum and the dorsal aspect of the spinal cord, and becomes confluent with the intravertebral venous plexus.

Moreover, as in ratites, the occipital sinus is formed by an anastomotic sinus connection in the caudal cranial fossa between the rostral semicircular vein and the dorsal sagittal sinus.

This anastomotic sinus courses from the rostrodorsal aspect of the rostral semicircular vein, 70 and travels caudodorsally across the endocranial aspect of the parietal-supraoccipital suture to the dorsolateral aspect of this suture where the sinus drains into the ventrolateral aspect of the dorsal sagittal sinus.

Basilar Sinuses

A slender venous sinus, the basilar sinus, drains the median rostroventral aspect of the medulla, on the dorsal aspect of the basisphenoid caudal to the caudoventral aspect of the dorsum sellae, and just medial to the basisphenoid fenestra. The lateral basilar sinus originates from the coalescence of a plexus of veins that drains the rostroventromedial medulla. The sinus travels caudolaterally across the basisphenoid, then across the pericranial lining of the dorsal aspect of the basisphenoid-basioccipital suture, and finally across the dorsolateral aspect of the basisphenoid en route to the ventromedial aspect of the metotic fissure. Early in its course, the basilar sinus receives the abducens vein. The abducens vein drains from the orbit into the endocranial cavity through the abducens canal and then the internal abducens foramen. The vessel then travels caudoventrally from the foramen, across the caudal face of the dorsum sellae, and then between the basisphenoid and the medulla to drain into the rostrolateral aspect of the basilar sinus.

Throughout its caudolateral path, the basilar sinus receives a dense series of tributaries draining from the medulla. The basilar sinus becomes increasingly plexiform through its course. The number of vessels draining into the basilar sinus becomes particularly dense along the basioccipital, where the vessels anastomose across the bone to form a dense venous plexus across the ventral medulla, and essentially form a single large plexiform basilar sinus. Laterally, the basilar sinus system drains into the metotic sinus. The metotic sinus-basilar sinus confluence forms a single caudally directed sinus that drains 71 across the ventral aspect of the otic capsule, then courses caudodorsally along the caudoventral aspect of the otic capsule and drains into the ventrolateral aspect of the occipital sinus along the internal rostrodorsal aspect of the foramen magnum. Laterally, the metotic sinus drains into the jugular venous system.

The Accessory Nerve and the Dural Venous Sinuses

In ratites and galloanserines, the spinal division of the accessory nerve (CN XI) travels cranially across the ventromedial aspect of the vertebral canal and the ventrolateral aspect of the spinal cord, and further rostral, travels across the dorsolateral aspect of craniovertebral joint capsule. At the endocranial ventrolateralmost aspect of the exoccipital, just rostral to the internal aspect of the foramen magnum, the spinal division of CN XI becomes confluent with a large triangular swelling (with the spinal division characterizing the caudally facing apex of the triangle) of CN XI. A branch off the ventrolateral aspect of the medulla travels laterally to, and becomes confluent with, the mid (almost ventral) medial aspect of the triangle. The large internal foramen for the caudal hypoglossal nerve is in the internal caudal aspect of the exoccipital in a position just medial to the CN XI triangular swelling. The caudal hypoglossal nerve courses laterally, and passes across the ventral aspect of the swelling to enter the foramen along the swelling’s medial aspect. Rostrally, the triangle bifurcates into dorsal and ventral rami in a position just caudal to the caudal hypoglossal nerve. The dorsal ramus travels rostrodorsally to a semilunar shaped fossa

(caudally concave) located in the caudomedial face of the endocranial aspect of the opisthotic and in a position just rostral to the internal dorsal aspect of the opisthotic- exoccipital border, caudodorsal to the caudodorsal aspect of the metotic fissure and caudal to the endolymphatic foramen and the caudoventral aspect of the cerebellar auricular fossa. 72 The dorsal ramus of CN XI terminates in the semilunar fossa, and then sends off branches

into a scattering of small foramina in the fossa which then course through canals within the

opisthotic. The ventral aspect of the fossa is confluent with a groove in the opisthotic,

caudoventrolateral to the otic capsule, and that curves rostrolaterally across the roof of the

metotic fissure. Within this groove is a series of foramina through which the branches of

the dorsal ramus of CN XI pass through, and then enter the dorsomedial aspect of the

metotic fissure.

The accessory nerve is an important landmark in that the rostroventrolateral aspect

of the occipital sinus ends at the dorsal aspect of the nerve’s dorsal ramus. Caudal to the

dorsal ramus, the ventrolateral border of the occipital sinus ends at the dorsal aspect of the

CN XI swelling, and caudal to the swelling, the ventrolateral border of the sinus rests against

the spinal division of CN XI within the rostral aspect of vertebral canal.

In galloanserines, an elongate and robust mound-like protuberance extends from the

ventral aspect of the exoccipital. The dorsal aspect of the protuberance extends from and

along the caudolateral aspect of the metotic fissure. This mound could not be identified in ratites. The metotic fissure is typically obliquely oriented, in a caudodorsal to rostroventral plane, and thus is the protuberance. The smaller middle and rostral internal hypoglossal foramina are located in the ventrolateral aspect of the mound. The ventral ramus of CN XI courses rostroventrally, and passes across the lateral aspect of the mound in a position just dorsal to the rostral two XII nerves and foramina. Rostral to the mound, the ventral ramus continues to course rostrally, and appears to exit from the endocranium through a small fissure(s) in the suture between the internal aspects of the rostroventral exoccipital, the dorsolateral basisphenoid, and the caudoventral prootic. 73 The metotic sinus courses along the caudal wall of the fissure (formed by the exoccipital), and flows out of the fissure into the endocranium and then to the area caudolateral to the fissure. The entire ventral aspect of the metotic sinus becomes confluent laterally with the large, expansive caudal component of the basilar sinus. The caudoventral aspect of this anastomosis courses caudodorsally across the bony pillar of the exoccipital between the metotic fissure and the caudal hypoglossal foramen. In this course, the sinus travels across the medial aspects of the ventral aspect of the dorsal ramus of CN XI and the rostrodorsal aspect of the CN XI swelling, and across the rostral aspect of the caudal hypoglossal foramen, and then drains into the caudoventrolateral aspect of the occipital sinus in a position just dorsal to the CN XI swelling. Immediately upon receiving the basilar

+ metotic sinus, the occipital sinus sends off a branch that passes ventral to and then into the caudal hypoglossal foramen, which then courses ventrolaterally along the roof of the caudal hypoglossal canal and the dorsal aspect of the caudal hypoglossal nerve. The ventral aspect of the occipital sinus sends off additional and large ventral branches that course around the caudal CN XII foramen which anastomose ventral to the foramen and then travel ventromedially across the internal caudalmost aspect of the exoccipital and just rostral to the rostroventrolateral border of the foramen magnum. This last sinus then courses across the caudal aspect of the floor of the endocranium and the foramen magnum just rostral to the dorsal aspect of the occipital condyle and medially becomes confluent with the contralateral sinus. Through these last ventral branches, the occipital sinus and its tributaries completely surround the inner circumference of the foramen magnum (Baumel 1975, 1993), as the foramen magnum sinus. The ventral component of the foramen magnum sinus is rostrally continuous with the plexiform basilar sinus system. 74 Endolymphatic Sac

The endolymphatic sac in galliforms and ratites extends from the rostrolateralmost aspect of the endolymphatic foramen. The endolymphatic foramen has a caudodorsally oriented opening. The opening is bordered dorsally, rostrally, and ventrally by the caudodorsal aspect of the prootic, and caudally by the rostrodorsal aspect of the opisthotic.

In juvenile galloanserines and ratites there is a fissure caudodorsal to the rostral semicircular eminence, which is bordered ventrally by the sutural area between the caudodorsal opisthotic and the rostrodorsal aspect of the exoccipital, caudally by the sutural contact of the rostrodorsal aspect of the exoccipital and the rostroventral aspect of the supraoccipital, dorsally by the rostroventral aspect of the supraoccipital, and rostrally by the rostroventral aspect of the supraoccipital and the caudodorsal aspect of the prootic. The endolymphatic sac expands out from its origin along the endolymphatic foramen and inserts laterally along the above described bony borders of the sac. In juveniles, a membrane stretches across the space within the fissure and forms the floor of the endolymphatic fossa. In later stages, the membrane ossifies. It is likely that the ossified membrane is the avian epiotic bone. In adults, the bony endolymphatic fossa is caudal to the caudoventral aspect of the rostral semicircular eminence, and dorsal to the semicircular fossa of the accessory nerve. In Anser, the endolymphatic fossa is much shallower, if not flat. The rostroventral aspect of the occipital sinus, in the area dorsal to the dorsal ramus of the accessory nerve, ends at the caudal aspect of the endolymphatic sac.

Cerebellar Auricular Fossa and Sinuses

The cerebellar auricular fossa is a deep fossa located within the rostrodorsal face of the otic capsule, in a position caudodorsal to the facial-internal acoustic meatus, and is 75 ventrally separated from the dorsomedial aspect of the metotic fissure by a horizontal, columnar structure formed by processes from a caudoventral aspect of the prootic and the ventrocaudal aspect of the supraoccipital, which contact and form a vertically oriented suture in the middle of the column. This column forms the ventral border of the cerebellar auricular fossa. The rostroventral border of the fossa is formed by a caudal aspect of the prootic, and the caudoventral aspect of the fossa is partially formed by the rostroventral aspect of the supraoccipital that is continuos with the rostroventral process of this bone that forms the caudoventral border of the fossa. The rest of the fossa is bordered by the rostral semicircular eminence, which appears as an inverted U-shaped protrusion from the dorsal aspect of the otic capsule. The rostroventral aspect of the eminence is formed by the caudodorsomedial aspect of the prootic, and acts as a the rostrodorsal border of the cerebellar auricular fossa. The dorsal aspect of the eminence and the dorsal border of the cerebellar auricular fossa is formed by the ossification of tissue between the endocranial caudodorsal aspect of the prootic and the rostrodorsal aspect of the supraoccipital. The caudodorsal aspect of the fossa is formed by the rostral aspect of the supraoccipital. The cerebellar auricle projects caudolaterally from the cerebellum and rests within the cerebellar auricular fossa. The auricle has a dense blood supply and is surrounded by venous sinuses.

The dorsal auricular sinus courses medially across the roof of the cerebellar auricular fossa and the dorsal aspect of the cerebellar auricle, and emerges into the endocranium at the dorsal aspect of the fossa. The sinus then turns and travels rostrodorsally across the lateral aspect of the bony dorsal border of the fossa. Dorsal to the rostral semicircular canal the sinus courses across the lateral aspect of the bony rostral semicircular vein canal, and then passes rostrodorsally to the ventromedial face of the protuberantia tentorialis. The sinus 76 then drains across the lateral aspect of the marginal crest and eventually empties into the ventrolateral aspect of the torcular herophili.

The ventral auricular sinus travels across the ventral aspect of the auricle and the dorsal aspect of the floor of the cerebellar auricular fossa, which is formed by the dorsal aspect of the supraoccipital process of the prootic. Upon entering the endocranial cavity, the ventral auricular sinus bifurcates into rostral and caudal sinuses. The ventral sinus drains caudoventrally across the lateral aspect of the ventral border of the cerebellar auricular fossa, toward the caudodorsal aspect of the metotic fissure, and upon reaching the fissure, the vessel drains into the caudodorsal aspect of the metotic sinus.

The rostral branch of the ventral auricular sinus drains rostroventrally along the lateral aspect of an obliquely oriented ridge (caudodorsal to rostroventral) of the prootic that separates the otic capsule from the mesencephalic fossa, and dorsal to the internal acoustic meatus. In a position along the ridge that is rostral to the internal acoustic meatus, the sinus receives a vein that drains from the fossa and across the rostrolateral aspect of the otic capsule. This vein receives veins that drain from the canals of the various vestibulocochlear nerves, and thus drains the inner ear. The rostral branch of the ventral auricular sinus then drains rostromedially across the fossa in the rostral aspect of the prootic, and drains into the trigeminal vein to form the rostral petrosal sinus in a position caudodorsal to the internal trigeminal foramen.

Within the caudal aspect of the cerebellar auricular fossa, the dorsal and ventral auricular sinuses and the other veins of the auricle combine into a single sinus that travels to and enters the auricular foramen. The auricular foramen, a ubiquitous structure in

Archosauria, is located in the caudoventralmost aspect of the cerebellar auricular fossa of 77 birds. The auricular foramen leads to a bony canal for the auricular sinus that has a long and

tortuous course passing caudoventrally through the exoccipital, and exits into the external

occipital region through a very small foramen (or foramina) in a grooved area along the

medial aspect of the exoccipital, just lateral to the external caudoventrolateral aspect of the

supraoccipital, and in the transverse plane of the dorsal aspect of the foramen magnum. The

external occipital vein drains ventrolaterally along this exoccipital groove, and the auricular

vein(s) empties into it.

Cavernous Sinus

The walls of the hypophyseal fossa are completely surrounded by a large thick venous sinus, the cavernous sinus (Kaku 1959; Richards 1967; Baumel 1975, 1993), that envelops the outer circumference of the hypophysis. In Struthio and Anas, the rostral wall of the hypophyseal fossa is characterized by a smaller, yet deep fossa that extends the hypophyseal fossa rostrally, and that is occupied by a thick rostral extension of the cavernous sinus. In all birds examined in this study, the orbital foramen (or rostral and caudal orbital foramina) is located in the rostrodorsolateral aspect of the rostral wall of the hypophyseal fossa. The orbital vein drains caudally through this foramen from the ventral aspect of the orbit, and empties into the rostrolateral aspect of the cavernous sinus. That aspect of the cavernous sinus that rests against the rostral wall drains into the right and left aspects of the cavernous sinus that rest against the lateral wall of the hypophyseal fossa.

The oculomotor foramen opens into the dorsolateral aspect of the hypophyseal fossa, and the oculomotor vein drains from the orbit into the fossa through this foramen and immediately empties into the rostrodorsal aspect of the component of the cavernous sinus that rests against the lateral wall of the fossa. The sinus bifurcates caudolaterally. The 78 dorsal part drains caudally to the caudal aspect of the fossa where it becomes confluent with the contralateral sinus, and together form a large sinus that extends across the caudal wall of the fossa. The ventral part drains caudoventrally to the caudodorsal aspect of the floor of the fossa and becomes confluent with the contralateral ventral branch, and together form a sinus that extends across the caudal aspect of the fossa floor. The median ventral aspect of the cavernous sinus travels along the caudal wall of the fossa, then drains ventrally in the median dorsal aspect of the sinus along the caudal aspect of the floor of the fossa.

Caudally, the bone of the floor of the hypophyseal fossa slopes caudoventrally to form the rostral wall of an obliquely oriented canal in the basisphenoid through which the cerebral carotid arteries course toward the hypophyseal fossa. Ventrally, the canal is divided into the two cerebral carotid canals. The median caudal aspect of the sinus that rests across the caudal aspect of the fossa floor, bifurcates into the right and left cerebral carotid veins

(Richards 1967), which then pass caudoventrally through the canal and then into and through the cerebral carotid canals.

The caudal wall of the hypophyseal fossa is the rostral face of the dorsum sellae.

The dorsolateral aspect of the component of the cavernous sinus that rests against the caudal wall of the hypophyseal fossa drains caudodorsally to the dorsal aspect of the dorsum sellae and then drains caudolaterally, dorsal to the caudal encephalic artery, and across the dorsum sellae, to drain into the ventrolateral aspect of the trigeminal vein. Proximal in this path, the extension of the cavernous sinus sends off small, slender veins that course caudoventrally across the caudal slope of the dorsum sellae and drain into the trochlear vein and the lateral basilar sinus. However, the major drainage of the cavernous sinus occurs through the carotid veins. 79 Basicranial Fenestra and Notocordal Crest

Another venous sinus is associated with the basicranial fenestra. Birds are typically characterized by a basicranial fenestra (Parker 1866, 1870; De Beer 1937) which in adult specimens is a longitudinal elongate fissure that stretches across the median rostral aspect of the floor of the clivus, which is formed by the dorsal aspect of the basisphenoid. The rostral aspect of the fenestra is in the caudoventralmost aspect of the dorsum sellae. In juveniles, the medial aspects of the paracordal plates, which fuse to form the dorsum sellae in adults, do not contact each other, and the space between them forms the vertically elongate rostral aspect of the fissure (De Beer 1937; pers. obs.). In most specimens, the rostral aspect of the fenestra has a large to very small patent foramen that opens into a bony canal that travels rostrally through the ventral aspect of the dorsum sellae, and opens via a foramen in the caudal wall of the canal for the common encephalic arteries and the internal carotid veins

(which is located rostrodorsal to the cranial carotid canals and caudoventral to the hypophyseal fossa). The dorsum sellae is frequently highly pneumatic, and in a tinamou skull the canal for the venous sinus of the basicranial fenestra could be observed passing through it.

In several specimens studied, the basicranial fenestra is occupied by a wide, longitudinally oriented venous sinus, and the basilar artery courses caudally across the dorsal aspect of this sinus. Rostrally, the venous sinus of the basicranial fenestra passes through the aperture in the dorsum sellae, through the canal within the dorsum sellae, out of the rostral foramen and into the canal of the common encephalic arteries. The sinus then drains into the caudoventral aspect of the cavernous sinus, which rests against the rostral face of the dorsum sellae. Caudally, the basicranial fenestra slopes caudoventrally, and the 80 caudalmost aspect of the fenestra opens through an occasionally large foramen into the large pneumatic space within the basioccipital, which is occupied by a large air sac. The caudal, endocranial aspect of the venous sinus of the basicranial fenestra courses caudally through the foramen and into the sinus. Occasionally, an artery is seen to course through the fenestra with the venous sinus, and a thick tissue was observed within the fenestra (which could also be vascular). This tissue cannot be a remnant of the pharyngeal- neurohypophyseal tissue. The ventral aspect of the basisphenoid rests dorsal to the rostral aspect of the pneumatic space within the basiparasphenoid, which is caudally continuous with the space in the basioccipital. A fossa can be identified in the ventral aspect of the fossa, with a foramen (foramina) that opens into a canal that passes rostrodorsally to the ventral aspect of the hypophyseal fossa. This canal opens through an occasionally large rostrodorsally oriented foramen in the floor of the hypophyseal fossa. This canal and its associated foramina is likely the true remnant of a craniopharyngeal canal.

In most juvenile and adult birds studied, just caudal to the basicranial fenestra, beginning at the rostrodorsalmost aspect of the basioccipital, there is a longitudinal crest that extends across the median dorsal aspect of the basioccipital, here termed the notocordal crest (see De Beer 1937 for a discussion of this feature in avian embryos; Welman 1995).

One specimen of tinamou possessed only the rostralmost aperture for the basicranial fenestra, and the notocordal ridge extended rostrally across the length of the basisphenoid and to the aperture at the caudoventral aspect of the dorsum sellae. The crest, which is variably sized, cleaves slightly into the median furrow of the medulla, and the basilar artery travels caudally across the dorsal aspect of the crest. Throughout the ventrolateral aspect of the length of the crest are small foramina through which small veins pass and anastomose or 81 drain from the basilar venous plexus. The caudalmost aspect of the crest terminates as a

large, pyramidal, dorsally protruding eminence just rostral to the dorsal aspect of the

occipital condyle. Along the caudal face of this eminence are a horizontal series of foramina

through which veins pass and course caudally to the foramen magnum sinus. Veins that

drain through the crest also drain ventrally into the basicranial area, a pattern that is

discussed in more detail in the section on cephalic venous drainage. It is unclear if there is

any relationship between the veins within the notocordal crest and the sinus of the

basicranial fenestra.

Crocodilians have described as lacking a basicranial fenestra (De Beer 1937).

However, I have observed specimens that possess this feature, which is rostral to the

notochordal ridge. In an Alligator specimen, the notochordal ridge was cleft into right and left ridges by a groove.

Encephalic Arterial System After coursing through the cranial carotid canals, the two internal carotid arteries

anastomose into a horizontally oriented vascular structure, the intercarotid anastomosis, and

then sends off a rostrally directed vessel(s), the caudal hypophyseal artery that ramifies across

the caudal aspect of the hypophysis (Wingstrand 1951; Baumel 1975, 1993). As the

continuing branch of the cerebral carotid artery enters the hypophyseal fossa, the vessel is

rostrodorsally inclined and travels rostrally against the lateral aspect of the hypophysis and

the medial aspect of the lateral wall of the fossa. Toward the rostral border of the

hypophyseal fossa and the rostrolateral aspect of the hypophysis the cerebral carotid artery

divides into dorsal and rostral branches, the common encephalic artery and arteria orbitalis

(the internal ophthalmic artery of Richards, 1967; Baumel 1975, 1993), respectively 82 (Richards, 1967; Baumel 1975, 1993). The orbital artery, a small-diameter vessel, travels to the rostralmost aspect of the hypophyseal fossa and exits the fossa through the orbital artery foramen (Baumel 1975, 1993), located in the rostrolateralmost aspect of the rostral border of the fossa. Figure 6A and B depict the encephalic course of the internal carotid artery and its branches in lateral and dorsal views, respectively.

The common encephalic artery divides into rostral and caudal branches within the fossa (Richards, 1967; Baumel 1975, 1993), ventral to the sella turcica (defined here as the ridge separating the hypophyseal fossa from the remaining endocranial cavity). The rostral branch, the rostral encephalic artery, courses over the rostrodorsal border of the sella turcica, and then travels dorsally and slightly medially across the medial border of the laterosphenoid bone near its rostral aspect within the rostral aspect of the mesencephalic fossa, and courses against the rostral aspect of the mesencephalon. Early in its course, the rostral encephalic artery passes across the medial aspect of the oculomotor nerve in the vicinity of the nerve’s passage into the oculomotor foramen. Near the dorsal aspect of the mesencephalic fossa, the artery bifurcates into caudal and rostral branches, the caudal and common rostral cerebral arteries, respectively (Baumel 1975, 1993).

The common rostral artery travels rostrodorsally to the dorsalmost aspect of the mesencephalic fossa, just ventromedial to the intersection of the tentorial crest and the ridge that divides the parietal cerebral and frontal cerebral fossae, and divides into caudal and rostral branches, the middle and rostral cerebral arteries, respectively (Baumel 1975, 1993).

Proximal to its bifurcation, the common rostral cerebral artery sends off vessels that ramify across the dorsal aspect of the optic tectum (Baumel 1975, 1993). The middle cerebral artery courses dorsolaterally along this latter ridge, and travels between the frontal and parietal 83 cerebral lobes, until it reaches the vallecula. Upon reaching the vallecula, the artery divides

into rostral and caudal vallecular branches that travel along the vallecular crest. The rostral

vallecular artery travels between the wulst and the frontal cerebral lobe, whereas the caudal

vallecular artery travels between the wulst and the parietal cerebral lobe. Both vallecular

arteries give off long vessels that travel and ramify medially across the wulst and then course

across the dorsal surface of the wulst before anastomosing with the interhemispheric artery.

The rostral cerebral artery travels medially across the ventromedial border of the

fossa of the parietal pole of the cerebrum, traveling dorsal to the optic tract at its exit from

the endocranium through the optic foramen and subsequently divides into a dorsal and a

rostral branch. The dorsal branch, the frontal cerebral artery, first gives off a rostrodorsal

branch, the ventral olfactory artery, that passes rostrally onto the roof of the orbitosphenoid

(the ossified supraseptal cartilage). The dorsal aspect of the orbitosphenoid extends across

the floor of the fossa of the frontal pole of the cerebrum, and then rostrally as the floor of

the olfactory canal, along the ventral aspect of the olfactory tract. The ventral olfactory

artery travels rostrally across the dorsal aspect of the orbitosphenoid. Toward the rostral

end of the olfactory canal, the ventral olfactory artery turns dorsally and ramifies into a series

of vessels that form an anastomotic plexus with terminal vessels of the ethmoidal arteries

and veins. The next branch(es) off the frontal cerebral artery, along with some early

branches from the ventral olfactory artery, ramify across the medial aspects of the floor of

the frontal cerebral pole fossa, along the ventral aspect of the frontal lobe of the cerebrum.

The ventral branch off the rostral cerebral artery, the cerebral ophthalmic artery (Baumel

1975, 1993), twists ventromedially to an area just dorsal to the medial aspect of the optic foramen and exits through a foramen situated in the orbitosphenoid dorsomedial to the 84 optic foramen and dorsolateral to the bony septum dividing the optic foramina (Richards

1967; Baumel 1975, 1993).

The caudal cerebral artery travels caudodorsally along the medial aspect of the tentorial crest, and courses along the ventral aspect of the parietal pole of the cerebrum dorsal to the dorsal aspect of the optic tectum (Richards 1967). The artery follows the tentorial crest caudodorsally, as it turns into the protuberantia tentorialis, and then travels caudodorsally along the protuberantia tentorialis, in a position just lateral to the caudomedial aspect of the parietal pole of the cerebrum and lateral to the rostromedial aspect of the diencephalon, medial to the optic tectum. Along the dorsal aspect of this region, the caudal cerebral artery divides into caudal and dorsal branches (Richards 1967). The caudal branch travels caudodorsally along the diencephalon toward the caudoventrolateral aspect of the epiphysis and then divides into lateral and rostral branches .

The lateral branch courses rostrally along the ventrolateral aspect of the epipiphysis to the rostral aspect of the organ and then turns and courses dorsally along the rostral aspect of the epiphyseal stalk to the epiphysis body. The caudal branch travels medially sending off a caudoventral branch across the dorsum of the diencephalon and a caudomedial branch to the dorsal aspect of the habanula and the superior colliculus, and sending rostral branches rostrally across the base of the epiphyseal stalk.

The rostral branch of the caudal cerebral artery courses rostrodorsomedially across the caudomedial aspect of the parietal pole of the cerebrum to the caudodorsomedialmost aspect of the cerebrum where it meets with the contralateral artery and anastomoses with it to form the interhemispheric artery (Baumel 1975, 1993). The single median artery then courses rostrally through the dorsal aspect of the falx cerebri, between the cerebral 85 hemispheres, ventral to the rostrodorsal sagittal sinus, and sends off an array of lateral vessels that course laterally across the dorsal aspects of the cerebral hemispheres. Rostrally, the vessel courses rostrally between the dorsomedial aspects of the olfactory tracts, along the ventral aspect of the ridge that extends longitudinally across the roof of the olfactory canal.

As the olfactory bulbs receive the olfactory nerves, the interhemispheric artery bifurcates into right and left ethmoid arteries that course rostromedially out of the olfactory canal and into the orbit through the olfactory foramina.

Caudal Encephalic Artery

The caudal encephalic artery passes caudodorsally along the hypophyseal fossa, and then caudally over the caudolateral border of the sella turcica. Upon reaching the endocranial floor, lateral to the sella turcica, the artery divides into lateral and caudal branches (Richards 1967; Baumel 1975, 1993). The lateral branch, the ventral mesencephalic tectum artery, passes caudolaterally along the caudoventral border of the middle cranial fossa, passing first along the caudoventral aspect of the optic tectum, sending vessels to the organ (Richards 1967; Baumel 1975, 1993) and then past the trigeminal ganglion. Along the internal maxillomandibular foramen, the artery sends off a branch, the trigeminal artery, that courses laterally through the ventral maxillomandibular trigeminal canal, and supplies the musculature in the lateral aspect of the temporal space. The ventral mesencephalic artery then travels toward the rostral aspect of the ridge along the prootic that divides the mesencephalic cavity from the otic capsule, and then courses caudodorsally across this ridge along the lateral aspect of the rostral petrosal venous sinus. 86 Basilar Artery

The caudal branch of the caudal encephalic artery travels caudomedially just lateral to

the caudolateral border of the sella turcica, and then travels caudomedially across the ventral

aspect of the diencephalon and the dorsal aspect of the dorsum sellae to its caudodorsal edge

where the vessel anastomoses with the contralateral artery to form a single median vessel,

the basilar artery (Richards 1967; Baumel 1967, 1975, 1993). In ratites the two caudal

branches that form the basilar artery are equal in size, whereas in Bonasa the right vessel is

much smaller, and in Anser the left vessel is much smaller. See Richards (1967) and Baumel

(1967) for a discussion of the asymmetry in the caudal encephalic artery. The basilar artery

courses caudoventrally along the median aspect of the caudal slope of the dorsum sellae and

sends off a series of vessels that course laterally across the rostral aspect of the

mesencephalon. The basilar artery travels to the caudoventralmost aspect of the dorsum

sellae and the rostroventralmost aspect of the mesencephalon. Caudal to the dorsum sellae,

the basilar artery courses caudally along the clivus, across the dorsal aspect of the sinus of

the basicranial fenestra, and the ventral aspect of the rhombencephalon, and sends off a

series of lateral vessels that course across the rhombencephalon. Proximal in this path, the

vessel passes along the ventrum of the pons and further caudal across the ventrum of the

rostral medulla (Richards 1967).

Caudoventral Cerebellar Artery

Dorsal to the basisphenoid-basiocciptal suture, the basilar artery sends of the large left and right caudoventral cerebellar arteries (the caudal ventral cerebellar arteries of Baumel

1993), which courses laterally across the suture for a short distance. The vessel then turns and courses caudolaterally across the rostrodorsal aspect of the basioccipital to the 87 ventrolateral aspect of the prootic. At the ventrolateralmost aspect of the prootic, the caudoventral cerebellar artery sends off a branch that travels rostrodorsally across the prootic and bifurcates into a rostral branch that travels toward the mesencephalic fossa, and a caudal branch, the rostral labyrinthine artery. The rostral labyrinthine artery travels caudodorsally across the prootic toward and into the rostroventral aspect of the internal acoustic meatus. The vessel then sends off a branch that travels rostrodorsally to and into the facial nerve foramen. The rostral labyrinthine artery then travels dorsally and sends off a rostral branch into the foramen of the lateral amupullary nerve, and distal to this, the rostral labyrinthine artery travels dorsally into the foramen for the rostral ampullary nerve.

After sending off the branch that gives rise to the rostral labyrinthine artery, the caudoventral cerebellar artery travels caudodorsally across the ventrolateral aspect of the prootic to the rostroventral aspect of the internal acoustic meatus, and sends off a series of vessels that ramify across the lateral aspect of the rhombencephalon in its course. The artery then sends off a rostrodorsal branch, the middle labyrinthine artery, that courses dorsally into the ventral aspect of the fossa. The middle labyrinthine artery sends off a branch into the foramen of the cochlear and lagenar nerves, and then travels dorsally into the foramen for the saccular nerve.

Upon sending off the middle labyrinthine artery, the caudoventral cerebellar artery curves along the caudoventral border of the internal acoustic meatus to the caudal border of the fossa and sends off the caudal labyrinthine artery that travels rostrally into the fossa and then into the foramen for the caudal ampullary nerve. After sending off this last artery, the rostrodorsal cerebellar artery courses caudodorsally to the caudodorsal aspect of the fossa and bifurcates into rostral and caudal branches, arteriae cerebellar auricularis and metoticis, 88 respectively. The metotic artery courses caudovenrally across the caudodorsolateral aspect of the prootic, and then the rostrodorsolateral aspect of the opisthotic and then into the dorsal aspect of the metotic fissure.

The cerebellar auricular artery courses rostrodorsally across the ventral border of the cerebellar auricular fossa, and then rostromedially into the fossa on the rostroventrolateral aspect of the cerebellar auricle. Richards (1967) discussed this aspect of the venous drainage of the auricle. The vessel then travels caudodorsomedially through the fossa along the rostrolateral aspect of the auricle and then bifurcates into caudal and rostral branches. The caudal branch travels caudally across the roof of the deep fossa and along the dorsum of the auricle. The rostral branch curves and travels in a tortuous rostromedial path along the roof of the fossa and bifurcates into rostral and caudal branches, arteriae cerebeller lateralis and cerebellar caudalis, respectively.

The lateral cerebellar artery travels rostrolaterally across the roof of the cerebellar auricular fossa and then exits the fossa at which point the vessel bifurcates into rostral and caudal branches, arteriae cerebellar rostrolateralis and cerebellar dorsolateralis, respectively. The former artery travels rostrodorsally along the rostrolateral aspect of the cerebellum, and then curves to the rostralmost aspect of the cerebellum, along the caudoventral aspect of the vertical dorsal component of the tentorial crest, and then ramifies across the rostral aspect of the cerebellum. The dorsolateral cerebellar artery curves dorsally between the parietal and the cerebellum and bifurcates into a ventral branch that courses caudodorsally along the lateral aspect of the cerebellum, and a dorsal branch that courses at a steeper caudodorsal angle across the cerebellum, along the lateral aspect of the transverse sinus, to the 89 dorsolateral aspect of the cerebellum and then curves laterally to course and ramify across

the dorsal aspect of the organ.

The caudal cerebellar artery courses caudally to and then laterally across the caudal

wall of the cerebellar fossa, and the caudal aspect of the auricle, to the caudolateral border of

the fossa. The vessel then travels caudally across the lateral aspect of the fossa’s caudal

border, then across the caudolateral aspect of the rostral semicircular eminence, and along the lateral aspect of the cerebellum. Finally, the caudal cerebellar artery curves medially along the caudolateral border of the cerebellum and ramifies across the caudal aspect of the organ.

After sending off the caudoventral cerebellar artery, the basilar artery continues to

course caudally across the median aspect of the endocranial canal, here formed by the dorsal

aspect of the basioccipital. In its course, the artery sends off a series of lateral vessels across

the ventral aspect of the medulla. In all birds studied, rostral to the atlantoocciptial joint

capsule, the basilar artery bifurcates into right and left arteries that course caudolaterally

across the joint capsule and anastomose with the intravertebral arteries. However, Richards

(1967) did not observe a connection between the basilar vertebral arteries in Gallus. I

identified such a connection in Gallus, Meleagris, Struthio, and Anas. The intravertebral

arteries travel rostrally along the ventrolateral aspects of the vertebral canal.

Tympanic and Temporal Regions

Stapedial Artery In galloanserines, there is a bony connection between the basisphenoid and the

metotic strut, and an additional bony connection between the alaparasphenoid and the

paroccipital process, known as the sphenoccipital bridge. The stapedial artery passes through 90 the space between the sphenoccipital bridge (jugamentum sphenoccipital) and the

“sphenometotic” bridge, and then passes rostrodorsally into a bony canal (Baumel 1975).

The entrance to this passage is lateral to the external glossopharyngeal and vagus foramina, and caudolateral to the external ostium of the cranial carotid canal. The medial wall of the canal is formed by the lateral aspect of the otoccipital. The stapedial canal is actually divided into rostral and caudal canals that separate the stapedial artery from the stapedial vein. In palaeognaths, there is not a true stapedial foramen, but rather the stapedial vessels course dorsally, across the lateral aspect of the otoccipital.

Acoustic Artery In Anas and Bonasa, upon exiting from the osseous stapedial canal, the stapedial artery bifurcates into ventral and dorsal branches, the acoustic artery and arteria temporoorbitalis, respectively. The acoustic artery supplies the cochlear and vestibular membranes, the columella, and other parts of the middle ear. A lateral branch of the acoustic artery (and vein) ramifies into a dense cavernous-tissue-like vascular plexus within a soft connective tissue along the caudal contour of the external auditory meatus and which attaches to rostrodorsal and ventromedial periosteum of this region. The tissue is additionally supplied by arteries derived from the rostral auricular artery that passes from the temporomandibular trunk and sends off caudal branches that course caudally across the tympanic cavity to the erectile mass. Additional veins drain from the ophthalmic rete, across the lateral aspect of the quadrate, and drain into the venous plexus of the acoustic tissue. A similar erectile-like tissue, supplied by the acoustic artery, is situated along the caudomedial floor of the tympanic cavity of ratites (Struthio and Dromaius), just rostral to the caudal tympanic recess. Erectile tissue in the middle ear, and drained by the acoustic vein, was 91 earlier identified in Gallus (Pohlman 1921), and in Pipilo by Beecher (1951), who proposed that the tissue functions to control air pressure during flight. However, I have identified erectile tissue supplied by the acoustic artery in the middle ear of flightless ratites, and in crocodilians (see Chapter 3)

Temporoorbital Artery In phasianids (e.g., Gallus and Meleagris), the temporoorbital artery is completely enclosed by an osseous tube, the tympanic canal, that passes dorsally through the middle ear region rostral to the paroccipital process, and which then turns and then courses rostrally, ventral to the ostium for the caudal tympanic recess. The vessel passes dorsal to the fenestra cochleae and vestibuli and thus the columella (Baumel 1975). The vessel passes ventral to the quadrate cotyla of the squamosal and dorsal to the otosphenoidal crest. This rostralmost area is laterally unossified in most chickens and adult turkeys. Rostrally, the otosphenoidal crest bends in medially to form the ventral aspect of the cranioquadrate canal. The squamosal capitulum of the quadrate comprises the lateral wall of the canal, and the dorsolateral aspect of the prootic forms the medial wall. In phasianids a long rostroventrally oriented process extending from the caudoventrolateral aspect of the squamosal, the temporal process, runs along the caudalmost aspect of the quadrate and contacts the caudodorsalmost aspect of the otosphenoidal crest. The temporal process separates the quadrate from the tympanic region. Dorsally the tympanic process forms the rostrolateral border of the ostium into the dorsal tympanic recess, and ventrally the process forms the caudolateral border of the caudal ostium to the cranioquadrate canal. Rostral to the rostromedialmost aspect of the squamosal capitulum of the quadrate, the temporoorbital vessels exit the cranioquadrate canal and enter the dorsal temporal region. 92 The temporoorbital artery immediately bifurcates into a rostral and caudal branch,

arteria profundotemporalis and the external occipital artery. The external occipital artery curves

caudally around the otic capitulum of the quadrate and enters a small foramen dorsal to the

cotyle, which leads into an osseous tube for the occipital artery that passes through the floor

of the dorsal tympanic recess. In galloanserines, the entrance to the dorsal tympanic recess

is situated caudolateral to the space between the otic and squamosal capitulum of the

quadrate. The external occipital artery foramen is situated between the caudoventromedial

aspect of the squamosal, the caudodorsal aspect of the paroccipital process, the

caudoventrolateral aspect of the supraoccipital, and the caudoventrolateral parietal . Upon

reaching the dorsal cervical region from the external occipital foramen, the external occipital

artery courses dorsally across the sutural contact of the caudomedial aspect of the squamosal

and the caudolateral aspect of the supraoccipital, and along the rostrolateral aspect of m.

splenius capitis. The vessel travels to the rostroventrolateral aspect of m. complexus and

then proceeds to course caudally along this aspect of the muscle, and anastomoses with

branches from the dorsal deep occipital artery that supply m. complexus.

In anseriforms, Struthio, Dromaius, and tinamous the temporoorbital artery and vein are enclosed by bone only in the caudoventralmost aspect of their dorsal course through the caudomedial aspect of the tympanic space. This short bony canal is a longitudinally wide structure with the appearance of a volcanic caldera (more so in anseriforms) and is the dorsal and tympanic component of the stapedial canal. In all these forms, the dorsomedial wall of the stapedial canal is formed by an extension of the exoccipital, and the lateral wall appears to form from a dorsal extension of the parabasisphenoid. The vessels pass through a fleshy

(cartilage-like) tube that arises from the tympanic ostium of the stapedial canal and then 93 extends dorsally toward and then dorsolaterally across the medial aspect of the ostium into the caudal tympanic recess. The tympanic process of the squamosal in anseriforms is short and non-existent in palaeognaths, and a long and thick otic capitulum of the quadrate extends caudomedially from the caudodorsomedial aspect of the quadrate and articulates with the otic quadrate cotyla, which is the rostral face of a stout rostroventral process, the pila otica, of the lateral aspect of the otoccipital. The otic-quadrate joint forms a broad ventromedial border for the ostium into the dorsal tympanic recess, and the fleshy stapedial canal rests against the medial aspect of the joint.

Rostral to the fenestra vestibuli, there is a bony cranioquadrate canal for the passage of the temporoorbital artery. The entrance to the canal is through an ostium between the dorsomedial aspect of the otic quadrate cotyla, the dorsomedial aspect of the otosphenoidal crest, and the caudodorsolateral aspect of the prootic. The caudalmost aspect of the cranioquadrate canal is formed by the otic quadrate cotyla, which comprises the dorsal portion of the canal, the otosphenoidal crest arches caudodorsally toward the dorsal tympanic recess and forms the ventral aspect of the canal, and the laterosphenoid forms the medial wall of the canal. Further rostral, the otic capitulum of the quadrate forms the rostralmost aspect of the cranioquadrate canal. The vessels exit the canal through an ostium formed laterally by the rostromedial aspect of the squamosal capitulum of the quadrate in anseriforms (the otic condyle of the quadrate in palaeognaths), medially by the dorsomedial aspect of the prootic, and ventrally by the rostrodorsalmost aspect of the otosphenoidal crest.

In anseriforms, the external occipital artery and vein enter a well developed bony canal, which opens caudoventromedial to the squamosal capitulum of the quadrate and is 94 occasionally closed laterally by a bony process that extends dorsolaterally from the lateral

aspect of the prootic and then attaches to the ventromedial aspect of the quadrate cotyla of the squamosal and the dorsolateral aspect of the squamosal capitulum of the quadrate, all of which forms a foramen and closed canal. In ratites, the vessels pass caudodorsally through a groove rostrodorsomedial to the otic condyle. The external occipital vessels then run caudodorsally medial to the ostium into the dorsal tympanic recess and then pass into the recess. In anseriforms, the vessels course through a tube in an arc (the arc has a rostroventral to caudodorsal orientation) across the space within the dorsal temporal recess before exiting into the external occipital region through the external occipital artery foramen.

In palaeognaths, the vessels immediately pass into a foramen in the floor of the dorsal

tympanic recess, which is formed by the dorsal aspect of the prootic, and then passes

through a canal in the floor of the recess before exiting through the external occipital artery

foramen.

Dorsal Aspect of the Temporal Fossa and the Profundotemporal Artery The profundotemporal artery exits the cranioquadrate canal into the dorsal aspect of

the temporal fossa in a position ventromedial to the tendon of m. adductor mandibulae

externus profundus pars caudalis (henceforth abbreviated as AMEPC), lateral to the

aponeurosis of m. adductor mandibulae profundus pars rostralis (AMEPR), and

caudodorsolateral to the mandibular nerve. The profundotemporal artery courses

rostroventrally toward the caudal aspect of the muscle body of AMEPR, and then bifurcates

into dorsal and ventral rami, arteriae profundus and lateral temporalis, respectively (illustrated in

Assenmacher 1953). See Table 2 for the terminology used for the jaw musculature in this

dissertation, and a list of commonly used synonyms. 95 Profundus Artery

The dorsal ramus of the profundotemporal artery, the profundus artery, immediately sends off a vessel that courses rostrocaudally along the caudolateral aspect of the laterosphenoid, and along the rostromedial aspect of the otic process of the quadrate and then bifurcates into caudal and dorsal branches. The caudal branch courses caudally across the lateral aspect of the squamosal capitulum of the quadrate, the dorsal aspect of the tendon of m. adductor mandibulae externus (AME) medialis and its tubercle, and the medial aspect of AMEPC. The vessel then travels to the thick connective tissue of the rostral border of the tympanic space and anastomoses with branches of the rostral auricular artery. The dorsal branch, the middle meningeal artery (Hafferl 1933) courses rostromedially, across the medial aspect of AMEPC. Distally, the vessel courses toward a series of foramina (usually two), including a large rostral foramen situated in the suture between the rostrodorsolateral aspect of the laterosphenoid and the rostrodorsomedial aspect of the squamosal. In galloanserines, these foramina are within the dorsal aspect of the temporal fossa, and, more specifically in anseriforms, the foramina are in the caudalmost aspect of the AMEPR fossa.

The middle meningeal artery breaks up and sends arteries into each of these foramina, which then open into the encephalic cavity in a position just dorsolateral to the tentorial crest. The vessels then ramify across the dura and deeply groove the bony walls of the cerebral fossa.

The profundus artery in Struthio sends off a series of vessels that pass through foramina in the dorsal temporal space within the rostrolateral squamosal and along the sutural contact between the rostroventral squamosal, the rostrodorsal laterosphenoid, and the caudoventral frontal in the rostrodorsal aspect of the dorsal temporal space. The ratite cerebral fossa is deeply grooved and a portion of these grooves are related to a series of foramina in the 96 external rostrodorsal laterosphenoid-caudoventral frontal suture within the orbit, and vessels from the supraorbital artery can be seen to pass out of the orbit through these foramina.

Rostral to sending off the middle meningeal artery, the profundus artery courses

rostrally across the dorsal aspect of AMEPR, but does not appear to send any branches into

the rete ophthalmicum. The profundus artery and vein then curve rostrodorsally away from

AMEPR, passing through a connective-tissue (similar in appearance to aponeurotic tissue)

sheet. Within this tissue, the vascular bundle passes between the caudalmost aspect of the

postorbital process, which is dorsal, and the pseudotemporalis process, which is ventral to

the bundle. Just beyond these two structures, the sheet becomes confluent with the

circumorbital membrane, and the vessels pass through the membrane into the caudolateral

orbit and divide into the ophthalmotemporal and supraorbital arteries and veins. The

supraorbital artery passes along the caudal and then dorsal aspect of the large lacrimal gland,

sending a dense array of vessels to the gland, which then anastomose and form the plexus of

the lacrimal gland.

Ophthalmic Rete

The rostrolateral aspect of AMEPR and the rostromedial aspect of AMEPC are

tightly and complexly connected by a large and thick aponeurosis that blends into each

muscle, and is more rostrally confluent with the rostral adductor aponeurosis that ensheathes

the rostral aspects of the adductor muscle mass. The rostral adductor aponeurosis spreads

from the rostrodorsomedial aspect of AMEPR to the rostrodorsolateral aspects of AME

superficialis, and then spreads rostroventrally across the rostral aspects of these muscles and

becomes rostroventrally confluent with the muscle’s tendinous and aponeurotic tissues that

insert into the mandible. 97 The ventral ramus of the temporoorbital artery, the temporal artery (Richards, 1967),

courses ventrolaterally along the caudodorsal aspect of AMEPR and gives off a caudodorsal

branch that ultimately courses through the tissue just dorsal to the external auditory meatus.

As the temporal artery continues to course ventrally along the caudal aspect of AMEPR, the

vessel sends off a series of caudally directed vessels that supply the adductor muscles deep

and caudal to the quadrate. At the same time, the artery sends off a dense series of rostrally,

rostrodorsally, and rostroventrally directed arteries that pass through muscle fibers of

AMEPR and into the thick aponeurosis between AMEPR and AMEPC and ramify

throughout the tissue to form a complex vascular physiological device, the ophthalmic rete.

The aponeurosis suspends the rete. This rete is characterized by a dense arterial and venous

plexus, and arteriovenous anastomoses (Midtgard 1984a). The ophthalmic rete can have the

appearance of two retia, in that it is really characterized by an external rete which is venous

and has a large vein associated with it, and is in close apposition to a medially placed arterial

rete.

In phasianids the rete is largely found within the tendinous section of AMEPR (in

Anas and Anser, this tendionous AMEPR appears to become muscle more dorsally and rostrally). Also, in palaeognaths, the rete is almost completely suspended within this aponeurotic tissue. In ratites, the aponeurotic tissue blends rostrally into the caudal aspect of the circumorbital membrane.

Upon emerging from the maxillomandibular foramen, the maxillary nerve passes

rostrally through the center of the ophthalmic rete and is completely surrounded by the retial

vessels. After passing through the rete, the maxillary nerve courses rostrally through the

adductor aponeurosis and then travels rostrally through the thick connective tissue, the 98 periorbital fascia, which spreads across the ventral aspect of the circumorbital membrane, and which is caudally confluent with the rostral adductor aponeurosis.

AME medialis covers the otic process and the caudal component of the quadrate

body, and continues along the rim of the fossa and across the articular crest of the

postorbital process—an aponeurotic sheet extending from this muscle is mainly lateral to the

rete, but the caudal aspect of the rete is covered primarily by musculature. M.

pseudotemporalis superficialis originates by a thin aponeurosis on a laterosphenoid tubercle,

medial to the postorbital process, and just ventrolateral to the profundus foramen, the

muscle passes obliquely, rostroventral to the medial aspect of the mandible where it inserts

into the rostral aspect of the pseudotemporal tubercle. The dorsolateral aspect of m.

pseudotemporalis superficialis rests against the ventromedial face of the dorsal aspect of

AMEPR and the aponeurotic component of the latter muscle, and so the ventromedial

aspects of the rete lies against the dorsolateral aspect of m. pseudotemporalis superficialis.

The rete is dorsal to m. adductor mandibulae caudalis.

The ophthalmic rete rests against the caudoventral aspect of the postorbital

process, just ventral to the coronoideus fossa and the articularis fossa, at the base of the

laterosphenoid component of the process. The medial aspect of the rete rests just against

the trigeminal foramen.

Lateral Aspect of the Temporal Space

Ventral Course of the Temporal Artery The temporal artery travels rostroventrally across the caudoventrolateral and then

the ventrolateral aspect of the rete, and sends off a series of rostrodorsal vessels into the

rete. The first large ramus of the temporal artery, arteria pseudotemporalis (which ultimately 99 supplies m. pseudotemporalis), branches from the ventromedial aspect of the former artery, along the caudoventral aspect of the ophthalmic rete. The main continuation of the temporal artery is here termed arteria orbitotemporalis. The m. pseudotemporalis artery courses ventromedially across the caudomedial and then medial aspects of the rete, and obliquely parallels the maxillary nerve. The artery immediately gives off caudolateral vessels to AME medialis, then gives off a series of dorsal branches to the rete and a ventral branch to m. pseudotemporalis superficialis. The m. pseudotemporalis superficialis artery travels caudally across the lateral aspect of the mandibular nerve toward the mandibular foramen, and then crosses over the dorsal aspect of the mandibular nerve to the point where the nerve gives off a branch that innervates mm. pseudotemporalis superficialis and retractor bulbi. The artery follows medially along the dorsal aspect of the m. pseudotemporalis superficialis ramus to supply m. pseudotemporalis superficialis, and both the artery and nerve send off dorsal branches that travel to m. tensor periorbitae and supply and innervate it. The terminal branches off the m. pseudotemporalis artery continue to travel across m. pseudotemporalis superficialis, and give off a medial vessel(s) into it.

At the rostrolateral aspect of the ophthalmic rete, the orbitotemporal artery bifurcates into a dorsal and ventral branch, the infraorbital artery and ramus muscularis, respectively (Assenmacher 1953; and in Gallus, Richards 1967). The infraorbital artery courses dorsally (Assenmacher 1953) across the rostral aspect of the rete and sends off a series of caudal vessels into it. At the rostrodorsolateral aspect of the rete, the infraorbital artery turns and then courses rostrally, through the ventral periorbital fascia lateral and parallel to the maxillary nerve (Assenmacher 1953), and sends off dorsally branches to m. 100 tensor periorbitae and lateral branches that ramify across the medial aspect of the ventral eyelid (Baumel 1975).

The muscular ramus of the temporal artery then continues to course rostroventrally, following along the lateral aspect of the mandibular nerve, and across the dorsomedial aspect of AME medialis. At the point the mandibular nerve gives off the rostromedially directed branch to m. pterygoideus dorsalis, the muscular ramus bifurcates into medial and lateral branches, the m. pterygoideus dorsalis and internal mandibular arteries, respectively. The m. pterygoideus dorsalis artery then gives off a branch that passes rostromedially to the dorsal aspect of the mandibular nerve, then passes rostromedially over the dorsal aspect of the mandibular nerve to the medial aspect of the nerve, then follows along the medial aspect of the mandibular nerve, and subsequently along the medial aspect of the nerve ramus to m. dorsal pterygoideus. In its course along this nerve, the neurovascular bundle passes medial and then rostral to the AM caudalis tubercle, then courses between AMEPR and AM caudalis, with the nerve innervating them. The artery supplies, in caudal to rostral order, mm. protractor quadratus, AMEPR, AME caudalis, and finally pterygoideus dorsalis.

The intramandibular artery continues to travel rostrolaterally and in its course supplies the medial aspects of the zygomaticus and superficialis components of AMEPR before passing to the mandible, and supplies the tendinous and muscular fibers of AMEPR as they insert into the coronoid process. The terminal branch of the vessel passes medially across the mandible with the mandibular nerve and enters the mandibular foramen

(Midtgard 1984a; and in Gallus, Baumel 1975, 1993) where it anastomoses with the mandibular artery, and then courses through the internal mandibular canal, sending off a series of laterally oriented nutrient vessels that supply the dermis of the mandible, and which 101 anastomose with branches of the external mandibular artery which enter the mandible through a series of longitudinal foramina within the external mandibular groove.

Postorbital Plexus In Meleagris and Gallus, the profundus artery trifurcates into the supraorbital, ophthalmotemporal, and postorbital arteries. The postorbital artery courses laterally across the rostral aspects of AMEPR, AMEPC, and finally the zygomaticus and superficialis components of AMEPR. At its lateral extent the postorbital artery and vein become plexiform and course laterally across the rostrodorsal aspect of the postorbital ligament where the vessels send off caudally oriented branches across the lateral aspect of the postorbital ligament. The caudal branches anastomose freely with a plexus of vessels derived from the temporomandibular and external carotid arteries. The maxillary artery, along the rostroventrolateral face of the quadrate, sends off a branch that courses rostrodorsally toward the postorbital ligament, and then ramifies across the ligament’s dorsolateral face.

The temporomandibular vessels anastomose more caudally with the vessels derived from the external carotid artery. The resulting plexus on the dorsolateral postorbital ligament has the appearance of a rete, with a dense venous rete just lateral to an arterial rete. The anastomosis between these retia and the plexiform branches of the postorbital artery and vein form a large and extremely dense plexus medial to the rostral aspect of the postorbital ligament, which completely fills the caudodorsal orbit. Medially, the plexus extends to anastomose with a series of vessels derived from the supraorbital artery, and the lateral aspect of the plexus continues rostrally to form a plexus that spreads throughout the dorsal palpebra. With the dorsal palpebra, the lateral wall of the orbital space presents itself as a complex vascular plexus. 102 Trigeminal Artery Within the rostroventral aspect of the mandibular component of the maxillomandibular canal, the trigeminal artery bifurcates into rostral and caudal branches.

The rostral branch exits the maxillomandibular foramen and travels rostrolaterally across the rostroventral aspect of the mandibular nerve, and then bifurcates into dorsal and ventral branches. The dorsal branch travels dorsally around the rostral aspect of the mandibular nerve and then courses rostrodorsally toward, and then passes through and ramifies within

AMEPR. The ventral branch courses rostroventrally away from the nerve, travels to m. pseudotemporalis superficialis, and ramifies across and within the muscle.

The caudal branch of the trigeminal artery courses caudoventrally across the caudoventral aspect of the mandibular nerve to the nerve’s caudoventralmost aspect and then bifurcates into dorsal and ventral branches. The ventral branch courses caudoventrally across the caudoventrolateral aspect of the prootic, medial to the orbital process of the quadrate, and across the caudomedial aspect of AM caudalis. The dorsal branch travels caudodorsolaterally across the caudal aspect of the mandibular nerve, and anastomoses with the infraorbital artery.

Orbital Region

Myology and Osteology of the Orbit In galloanserines, a robust protuberance on the laterosphenoid extends from the lateralmost aspect of a medially oriented ridge that extends along the length of the ventromedial aspect of the postorbital process. M. tensor periorbitae has a tendinous insertion into this, the m. tensor periorbitae process. Rostroventral to the m. tensor periorbitae process, is a second robust process, the m. pseudotemporalis process, from 103 which a tendon of m. pseudotemporalis inserts. This second process is located rostral and slightly dorsal to the maxillomandibular foramen.

Just caudal to the profundus foramen, is a variably sized, rostroventrally oriented, protuberance that originates from the rostromedial face of the external aspect of the laterosphenoid, the m. rectus lateralis process. A thick ridge, the dorsal orbital crest, extends from the dorsolateral aspect of the process and courses laterally across the laterosphenoid and becomes confluent with the m. tensor periorbitae process.

A second ridge, the ventral orbital crest, extends from the rostralmost aspect of the m. pseudotemporalis process and travels medially across the laterosphenoid ventrally parallel to the dorsal orbital ridge. Medially, the dorsal and ventral orbital crests course toward one another and become confluent, and extend rostroventromedially as a single process, the above mentioned m. rectus lateralis process. The tendon of m. rectus lateralis originates from the dorsal aspect of the m. rectus lateralis process, whereas m. pseudotemporalis has a strong tendinous insertion on the ventral aspect of the m. rectus lateralis process. M. pseudotemporalis has another horizontally oriented tendon that inserts along the length of the ventral orbital ridge. M. tensor periorbitae has a caudoventrally oriented tendon that inserts across the length of the dorsal orbital ridge.

The dorsal aspects of the circumorbital membrane are continuous with the tendon(s) of m. tensor periorbitae, and so extend from the length of the dorsal orbital crest, and more laterally from the m. tensor periorbitae process. The dorsal orbital crest thus defines the caudoventral orbital margin. Dorsolateral to the m. tensor periorbitae process, the circumorbital membrane extends dorsolaterally across a fossa in the medial face of the postorbital process that defines the caudolateral orbital margin. 104 Both the ventral orbital crest running along the postorbital process and the dorsal

orbital crest that is confluent with it protrude from the laterosphenoid, and this entire dorsal

ridge system can be seen to run from the caudoventral laterosphenoid bone to its more

rostral aspect. The dorsal ridge system actually acts to separates the temporal and orbital

regions. Caudoventral to the postorbital component of this ridge is the coronoideous fossa

where AMEPR, the medialmost AME muscle, rests, whereas the circumorbital membrane is

rostrodorsal to this ridge. Moreover, m. pseudotemporalis, a temporal muscle, rests ventral

to the dorsal orbital ridge, and the circumorbital membrane rests dorsal to the ridge. This

dorsally placed ridge system is almost identical to the cotylar crest, which is described in

crocodilians (Chapter 3), and which is found in most, if not all, fossil non-ornithurine

dinosaurs (e.g., Allosaurus, Deinonychus).

In anseriform specimens with a well ossified orbitosphenoid, a strong vertically

oriented ridge protrudes from the orbitosphenoid in an area rostrodorsal to the oculomotor

foramen and along the caudoventral aspect of the optic foramen. Occasionally, this strong

ridge is continued ventrally by a more slender ridge that passes across the area rostral to the

oculomotor foramen. The dorsalmost aspect of the ridge, which is nearest the optic

foramen, is a strong, rostrolaterally inflected process. The tendon of m. rectus dorsalis

attaches to the dorsal aspect of the ridge and its dorsal process. The tendon of m. rectus

ventralis inserts along the rostroventrolateral aspect of the ridge. The anatomy of this ridge

in Rhea is almost identical to that described for anseriforms.

In Struthio, the orbitosphenoid is not as well ossified, and the area of the above discussed system of orbital ridges is developed as a robust process that forms, or is formed by, the rostral bony border of the confluent oculomotor and abducens notches. The process 105 is located rostrodorsal to the orbital artery foramen and forms the caudoventral border of the optic foramen. This process is characterized by two smaller processes: a dorsally inclined process from the dorsal aspect of the more robust process and a laterally inclined process extending from the lateral aspect of the robust process.

Another ridge extends around the circumference of the rostrodorsal, rostral, and rostroventral aspects of the bony border of the optic foramen. Tendinous fibers of m. rectus medialis inserts into this semi-lunar shaped crest, the m. rectus medialis crest.

Additionally, in anseriforms a deep, caudomedially directed fossa is found in the orbitosphenoid in a position caudoventral to the cerebral ophthalmic artery foramen, and dorsal to the optic foramen. A caudodorsally directed extension of m. rectus medialis fills and inserts within this fossa. In ratites, a strong laterally projecting vertical ridge along the orbitosphenoid, between the ventral aspect of the cerebral ophthalmic artery foramen and the dorsal aspect of the orbital foramen, serves as a site of insertion for m. rectus medialis.

Also, in ratites specimens with a well ossified dorsal orbitosphenoid (e.g., Dromaius,

Casuarius), a strong vertical ridge protrudes from the orbitosphenoid just dorsal to the cerebral ophthalmic artery foramen, and the caudodorsal extension of m. medialis inserts along it.

The tendons of mm. obliquus ventralis and dorsalis share, and originate from, a common aponeurosis in the rostrodorsomedial aspect of the orbit. The dorsal aspect of the aponeurosis inserts along the length of the rostroventral aspect of the ventral ridge defining the olfactory sulcus, just caudal to the caudodorsal aspect of the mesethmoid.

Upon exiting the trochlear foramen, the trochlear nerve travels rostrodorsally to the caudodorsal border of m. rectus dorsalis and then courses rostrodorsomedially across the 106 dorsal aspect of the muscle to the dorsal aspect of m. quadratus membranae nictitantes. The nerve then travels across the dorsal aspect of m. quadratus membranae nictitantes toward m. obliquus dorsalis, and in this course the nerve travels across the dorsomedial aspect of the dorsal ramus of the ophthalmotemporal vein and, more rostrally, across the dorsomedial aspect of a vein draining from m. obliquus dorsalis. Finally, the nerve travels rostrodorsally to m. obliquus dorsalis.

The profundus nerve, upon exiting the profundus foramen, courses rostrodorsally across the ventrolateral aspect of the tendon of m. rectus dorsalis and along the ventral aspect of the profundus vein. Rostral to the tendon, the nerve travels medially across the ophthalmotemporal vein, dorsolateral to the point the vein anastomoses with the profundus vein. The profundus nerve then courses rostrally across the dorsal aspect of the optic nerve and the medial aspects of m. quadratus membranae nictitantes, along the dorsal aspect of the ophthalmotemporal vein. In this area, the nerve travels across the medial aspect of the dorsal ramus of the ophthalmotemporal vein as it anastomoses with the ophthalmotemporal and ophthalmic veins. Further rostrally, the nerve travels rostrodorsally across the dorsomedial aspect of m. rectus medialis, and finally, the nerve passes dorsomedially across the tendons of mm. obliquus ventralis and dorsalis en route to the nasal cavity and toward the dorsal nasal artery, vein, and olfactory nerve.

Upon exiting its foramen, the oculomotor nerve travels rostrally across the lateral aspect of the oculomotor vein, and further rostral, travels across the ventromedial aspect of m. rectus ventralis to the rostroventromedial aspect of the muscle where it meets with the ophthalmic vein. A ventral ramus of the oculomotor nerve travels along the caudal aspect of the vein en route to m. obliquus ventralis. 107 Harderian Gland In Anas, the Harderian gland is situated rostral to the optic nerve, rostromedial to m. rectus medialis, and rostrolateral to m. quadratus membranae nictitantes. Medially, m. obliquus dorsalis is rostromedial to the gland, and laterally, the muscle is caudodorsal to the gland. Rostrally, m. obliquus ventralis is rostromedial to the Harderian gland and curves caudally to the ventrolateral aspect of the gland.

Venous Drainage and Arterial Supply of the Eye and Eye Musculature On the medial aspect of m. quadratus membranae nictitantes, near its origin from the bulbus oculi and dorsal to the optic nerve, is the “intersection” of three major vessels responsible for draining much of the orbital contents: the ophthalmotemporal, dorsal ramus of the ophthalmotemporal, and ophthalmic veins. Each of these veins drain into, or branches from, a large, semicircular, anastomotic vein that surrounds the dorsal, rostral, and caudal aspects of the optic nerve.

Dorsal Ramus of the Ophthalmotemporal Vein The dorsal ramus of the ophthalmotemporal vein drains ventrally, and slightly caudally from the origin of the nasal vein (Baumel 1975, 1993), just after the nasal vein is formed by the junction of the supraorbital and ethmoidal veins. The ophthalmotemporal vein passes first ventrally across the area of the orbitosphenoid ventral to the olfactory sulcus. The vein then passes caudoventrally across the dorsal aspect of the muscle of the nictitating membrane and lateral to m. obliquus dorsalis, and then continues to course caudoventrally between these two muscles before approaching the trochlear nerve. The vessel travels caudoventrally across and then past the medial aspect of the trochlear nerve, and then passes ventral to the ventral aspect of m. obliquus dorsalis, and continues to pass caudoventrally across m. quadratus membranae nictitantes. 108 Spreading across the area of the dorsal aspect of this muscle of the nictitating membrane is an extremely dense series of long, closely parallel vessels draining the caudodorsal aspects of the ciliary body, the caudodorsal ciliary plexus. The vessels of the caudodorsal ciliary venous plexus drain into a single vein (Hossler and Olson 1984), the caudodorsal ciliary vein, in an area dorsal to the trochlear nerve in its rostral passage between the muscle of the nictitating membrane and m. obliquus dorsalis. The caudodorsal ciliary vein travels caudoventrally, across the medial aspect of the trochlear nerve and then courses beyond the ventrolateral aspect of m. obliquus dorsalis. The caudodorsal ciliary vein continues in a caudoventral direction towards the ophthalmotemporal vein, and, in an area medial to m. quadratus membranae nictitantes, between the trochlear and the profundus nerves, the caudodorsal ciliary vein drains into the dorsal ramus of the ophthalmotemporal vein (Hossler and Olson 1984). After receiving the dorsal choroidal vein, the ophthalmotemporal continues in its course across m. quadratus membranae nictitantes and approaches the profundus nerve along the nerve’s course across this muscle. The vein courses caudoventrally across the medial aspect of the profundus nerve, and then travels across m. quadratus membranae nictitantes, curves ventrally and courses across the ventral muscular and then dorsal tendinous portions of the m. quadratus membranae nictitantes, and finally empties into the rostrodorsal aspect of the semicircular anastomotic vein.

Ophthalmotemporal Vein The ophthalmotemporal vein drains caudally from the ventrolateral aspect of the dorsal ramus of the ophthalmotemporal vein, in a position along the rostrodorsal aspect of the optic nerve (Richards 1967) and the dorsomedial aspect of m. quadratus membranae nictitantes. The vessels travels caudally across the optic nerve and m. quadratus membranae 109 nictitantes, and further caudal, courses across the dorsal aspect of these latter two structures and then across the ventral aspect of m. rectus dorsalis. Just caudodorsal to the optic nerve, in a position ventral to m. rectus dorsalis and on the dorsal aspect of m. quadratus membranae nictitantes, the ophthalmotemporal vein sends off a ventrally directed ramus that travels to an area between the caudal aspect of the optic nerve, the ventral aspect of m. rectus dorsalis, and the rostrodorsal aspect of m. rectus lateralis. The ventral ramus of the ophthalmotemporal vein then courses to the ventrocaudal aspect of the optic nerve, in an area rostroventral to m. rectus lateralis and caudodorsal to m. rectus ventralis, and then drains into the ophthalmic vein, which is discussed below.

Caudal to m. rectus dorsalis and the optic nerve, the ophthalmotemporal vein courses across the caudodorsal aspect of m. rectus lateralis toward the laterosphenoid. The vein then sends off a medially directed vessel to the laterosphenoid which bifurcates into rostral and ventral branches; the dorsal branch courses into the trochlear foramen and the ventral branch courses into the profundus foramen. Both of these latter vessels drain into the tentorial sinus.

Upon reaching the external rostromedial aspect of the laterosphenoid, in a position dorsal to m. rectus lateralis process, the ophthalmotemporal vein arches and travels caudodorsally to a point on the same transverse plane as the caudodorsal aspect of the postorbital process, and then arches and travels caudoventrolaterally and joins the supraorbital vein (Richards 1967, Richards termed the latter vessel the recurrent ophthalmic vein; Baumel 1975, 1993; Midtgard 1984a) to form the profundus vein.

Just ventral to its bifurcation into the ophthalmotemporal and supraorbital veins, the profundus vein anastomoses with a vein that courses caudoventrally. Both of these veins 110 travel just dorsal to the dorsal orbital crest, and the more ventral vessel travels across the dorsal aspect of m. tensor periorbitae. The proximal path of the ophthalmotemporal artery travels rostrodorsally between these large two veins and then travels laterally across the more ventral vein to the caudal aspect of the ophthalmotemporal artery, and immediately courses rostroventrally along the medial aspect of the ventral ramus of the ophthalmotemporal vein.

Ophthalmic Vein The rostrodorsal portion of the vein that anastomoses with the dorsal ramus of the ophthalmotemporal vein can be seen as the origin (or termination) of the ophthalmic vein.

The ophthalmic vein curves ventrally around the rostral aspect of the optic nerve to the nerve’s rostroventral aspect, and then continues to course ventrally to an area dorsal to the ventral division of the oculomotor nerve en route to the m. obliquus ventralis. At this point in the vessel’s course, the vein anastomoses with the ventral ramus of the ophthalmotemporal artery.

After coursing rostrally from an area between mm. rectus lateralis and ventralis, the ventral ramus of the ophthalmotemporal vein courses to the caudodorsal aspect of m. rectus ventralis and sends off a dense series of vessels that ramify across and drain the dorsomedial aspect of m. rectus ventralis and the ventral aspect of the optic nerve and eyeball. The vessel then extends rostrodorsally to the rostralmost aspect of the muscle and then courses rostrodorsally past the muscle, and then across the rostroventral aspect of the bulbus oculi.

Finally, the vein passes across the medial aspect of the ventral division of the oculomotor nerve, after which it continues rostrodorsally until it empties into the ophthalmic vein.

In its ventral course, upon passing medial to and then just past the ventral division of the oculomotor nerve, the ophthalmic vein immediately sends off a caudal branch that 111 passes caudally along the ventral aspect of the oculomotor nerve. In the area the

oculomotor nerve splits into its dorsal and ventral divisions, this vein splits into dorsal and

ventral branches, vena oculomotoris and the medial ramus of the orbital vein, respectively. This anastomotic relationship between the ophthalmic and orbital veins has been previously described (Richards 1967; Baumel 1975, 1993). The oculomotor vein travels caudodorsally

across the medial aspect of the oculomotor nerve, eventually arriving in a position on the

dorsal aspect of the nerve. The oculomotor vein ultimately passes through the oculomotor

foramen with the nerve, draining into the cavernous sinus.

The medial ramus of the orbital vein continues to pass caudally with, and along the ventral aspect of, the oculomotor nerve and along the caudolateral aspect of m. rectus ventralis. Before reaching the oculomotor foramen, the vessel curves ventrally away from the oculomotor nerve, partially around the ventrolateral curvature of m. rectus ventralis, after which the vein curves strongly in a ventrolateral direction and anastomoses with the lateral ramus of the orbital vein.

Dorsal to the foramen for the orbital vein is the ridge from which mm. rectus ventralis and dorsalis originates, and ventral to the foramen is the m. rectus lateralis process; the lateral ramus of the orbital vein is tightly positioned between these two ridges and the muscle bodies originating from them. This vein, which is a very large vessel, passes caudally between m. rectus lateralis and m. rectus ventralis before anastomosing with the medial ramus to form the orbital vein. Early in its course the lateral ramus passes caudomedially dorsal to the maxillary nerve, receiving caudal branches to the ophthalmic rete, and receiving more rostral veins draining from the ventral periorbital plexus. Vessels draining into the ophthalmic rete from the orbital vein are situated between mm. rectus lateralis and ventralis, 112 and anastomose with the previously mentioned veins that drain into the rete between mm.

rectus lateralis and dorsalis, effectively forming an anastomotic ring around m. rectus lateralis

and a venous plexus between this muscle and the lateral aspect of the eyeball. Along its

course the lateral ramus receives a dense array of veins draining mm. rectus lateralis and

ventralis so that much of the space between these two muscles is occupied by a venous

plexus. Finally, the vessel anastomoses with the medial ramus, forming the orbital vein,

which empties into the cavernous sinus (Richards 1967) after passing through the foramen

for the orbital vein. Often, a venous plexus can be seen surrounding the oculomotor

foramen, and the internal aspect of the oculomotor canal. A branch from the oculomotor

foraminal plexus drains ventrally to and then into the abducens canal. The abducens vein

then courses caudally through the canal, then into the endocranium through the internal

abducens foramen, and finally drains into the basilar and trigeminal sinuses.

After sending off the venous trunk of the oculomotor and orbital veins, the

ophthalmic vein resumes its rostroventral course toward m. obliquus ventralis, and travels

along the dorsal aspect of the ventral ramus of the oculomotor nerve. The vein and nerve

eventually pass to the ventromedial aspect of m. rectus medialis where the vein receives a

vessel that breaks up into several tributaries that drain from the muscle. Further rostroventral, the vein receives a large vein that courses rostrodorsally to the Harderian gland and which sends a dense of array of vessels into the extremely vascularized Harderian gland.

The ophthalmic vein then continues to follow along the dorsal aspect of the ventral ramus of the oculomotor nerve for a short distance and bifurcates into a rostral and caudal branch.

The caudal branch continues to travel with the ventral ramus of the oculomotor nerve to the dorsal aspect of m. obliquus ventralis and then ramifies across and drains the muscle. The 113 more rostral branch, which is the terminal branch of the ophthalmic vein, courses across the

medial aspect of m. obliquus ventralis, and then across the medial aspect of m. tensor

periorbitae toward the dorsal aspect of m. protractor pterygoidei et quadrati. The vessel

then courses ventrally across the lateral aspect of m. protractor pterygoidei et quadratis and

drains into the maxillary vein (Richards 1967; Baumel 1975, 1993; Midtgard 1984a), along the

dorsomedial aspect of m. pterygoideus dorsalis.

Orbital Branches of the Stapedial Artery Supraorbital Artery

The supraorbital artery curves along the coronoideous fossa on the ventral aspect of the postorbital process. The artery originally travels along the lateral aspect of the supraorbital vein, but later crosses rostrodorsally over the vein and then continues its course traveling along the vein’s dorsal aspect. The vessel then curves dorsally and runs caudally along the caudal aspect of the lacrimal gland into which the supraorbital artery sends a network of vessels, providing the gland with a dense blood supply. The lacrimal gland rests within a fossa on the dorsomedial aspect of the postorbital process, rostrodorsal to the ophthalmic rete. Dorsal to the lacrimal gland, the supraorbital artery curves rostrodorsally along the caudal aspect of the orbital margin (Assenmacher 1953, Richards 1967, Midtgard

1984a).

The Bony Orbital Margin The supraorbital artery travels rostrodorsally across the rostral face of the

caudoventral aspect of the bony orbital margin and continues to travel rostrally along the

bony orbital margin throughout much of its course. Moreover, the vessel often deeply

grooves the portions of the frontal that comprise the orbital margin. 114 The caudoventral orbital margin is formed by a vertical “ridge” along the

ventrolateral aspect of the frontal. Rostroventrally, this ridge is continuous with the

rostrolateral ridge across the laterosphenoid-parietal suture along the postorbital bar. Rostral to this ridge the frontal is deeply inflected medially, and forms the somewhat concave caudomedial orbital margin. Caudal to the orbital margin, the frontal is laterally inflated by the expanded cerebrum.

Further dorsal, the orbital margin curves steeply rostrodorsal across the frontal, and

forms the caudodorsal aspect of the orbital margin. From this area, the orbital margin

continues rostrally, and slightly ventrally, across the ventral aspect of the nasal process of the

frontal, and forms the bony, dorsal orbital margin. Medial to the dorsolateral orbital margin,

the frontal bone forms the orbital roof, and medial to this, forms the dorsomedial orbital

margin.

In the median plane of the dorsal orbit, the rostral face of the ventrolateral aspect of

the nasal process of the frontal is notched. The bone caudal to this notch is medially

inflected and becomes continuous with the more ventromedial surface of the nasal process.

Part of this medially inflected bone forms the caudal aspect of the dorsomedial orbital

margin. Rostral to the kink, the nasal process is rostrally continued by the dorsolateral

aspect of the frontal alone. The kink in the nasal process of the frontal represents the caudal

extent of the external olfactory foramen. Rostral to the external olfactory foramen, the

dorsal aspect of the orbital septum is dorsally elongated and medially inflected to articulate

with the ventromedial aspect of the nasal process of the frontal. Caudally, this medial

inflection of the septum articulates with the medial inflection of the frontal. As such, the 115 orbital septum becomes the medial wall of the olfactory groove that is formed by the

olfactory neurovasculature’s rostroventral course across the dorsomedial orbit.

Nasal Gland The nasal gland is a large, tubular gland that caudally rests just dorsal to the lacrimal gland and then fills the rostrolateral aspect of the caudolateral orbital margin, and, rostral to this, curves along the caudodorsal aspect of the orbital margin, and then across the ventrolateral aspect of the dorsal orbital margin. The gland terminates at the rostrodorsolateral aspect of the orbital margin, just caudodorsal to the mesethmoid.

The supraorbital artery travels against the caudomedial aspect of the nasal gland as the vessel courses dorsally across the caudoventral orbital margin. The vessel then travels along the medial aspect of the gland as it courses across the caudodorsal and dorsal orbital margins. Throughout the artery’s association with the nasal gland, the vessel sends off a vast array of arteries that form a dense arterial plexus throughout the gland’s substance. In specimens preserved as corrosion casts, the gross morphology of the gland is well represented by a vascular cast. Along the dorsolateral aspect of the orbital margin, caudolateral to the external olfactory foramen, the supraorbital artery bifurcates into lateral and medial branches.

The lateral branch of the supraorbital artery continues, as a smaller vessel, to travel across the rostrodorsomedial orbital margin and the medial aspect of the gland, then curves rostrolaterally with the curvature of the bony orbit across to the gland’s rostralmost extent, and then travels to a deep, caudally facing notch. The notch is formed by a space between the frontal process of the nasal bone and the lacrimal bone, just caudal to the sutural contact between these two bones. The artery then courses rostrodorsally through this notch, after which it enters and ramifies throughout the dermis of the scalp. 116 The medial branch of the supraorbital artery, which is much larger, becomes strongly

rostromedially inflected, and then courses rostromedially across the roof of the orbit toward

the dorsal aspect of the external olfactory foramen. The vessel then travels rostroventrally to

the pigmented meningeal tissue surrounding the olfactory neurovascular bundle and grooves

the frontal bone along this aspect of its course. The vessel then reaches the dorsal aspect of

the meningeal tissue, near the bundle’s entrance into the orbit from the external olfactory

foramen, and anastomoses with the ethmoid artery (Assenmacher 1953; Richards 1967;

Baumel 1975, 1993; Midtgard 1984a).

Ophthalmotemporal Artery

The ophthalmotemporal artery courses medially across the dorsal aspect of m. tensor periorbitae, the dorsal orbital ridge from which the muscle originates, against the rostral face of the caudoventral circumorbital membrane, ventral to the ophthalmotemporal vein, and just dorsal to another vein that runs parallel to it. The vessel turns rostrodorsally and courses toward the medial aspect of the eyeball. Early in its course, the ophthalmotemporal artery and the vein that travels ventral and parallel to it sends off a branch, the long ciliary artery and accomponying vein (Hossler and Olson 1984), that courses ventrolaterally across the dorsal aspect of m. tensor periorbitae and the caudomedial aspect of the bulbus oculi, then travels laterally across the dorsal aspect of m. tensor periorbitae and the caudoventral aspect of the bulbus oculi. According to Hossler and Olson (1984), the long caudal ciliary artery anastomoses with the iridial ring artery. The artery courses above the m. rectus lateralis process and then travels, with the ventral ophthalmotemporal vein, between mm. rectus lateralis and dorsalis where it gives off branches into the plexus located between these two muscles. 117 The ophthalmotemporal artery becomes ventrally oriented and courses in this

direction toward the eyeball. In its route, the artery passes rostrally across the dorsal aspect

of m. rectus lateralis and then rostroventrally between this muscle and m. rectus ventralis,

and again gives off branches into the plexus located between these two muscles. In this

region, the ophthalmotemporal artery anastomoses with the orbital artery (Richards 1967;

Baumel 1975, 1993; Midtgard 1984a), and the resulting vessel immediately gives off a long rostroventrally oriented vessel into the ciliary body, the caudoventral ciliary artery, that

ramifies into a dense series of long vessels that forms the caudoventral aspect of the choroid

plexus. The artery then runs rostrally across the dorsal aspect of m. rectus ventralis, and

across the ventral aspect of the optic nerve. Along the optic nerve, the ophthalmotemporal

artery sends off a vessel that travels into the eyeball with the optic nerve and then forms the

pectin oculi.

Beyond the rostral aspect of m. rectus ventralis, the artery travels rostrally to and

then across the ventrolateral aspect of the ophthalmic vein, where the vein divides into its

ventral continuation toward the maxillary vein and its dorsal branch into the Harderian vein.

On the rostrolateral aspect of the ophthalmic vein, the ophthalmotemporal artery sends off a

Harderian artery that travels across the lateral aspect of the Harderian vein into the

Harderian gland. Shortly, the Harderian artery divides into rostrodorsal and rostroventral

arteries that travel on the lateral aspects of the rostrodorsal and rostroventral veins through

the gland, and ramify into a dense plexus that supply it. After sending off the Harderian

artery, the ophthalmotemporal artery travels dorsally along the rostrolateral aspect of the

ophthalmic vein, toward the dorsal ramus of the ophthalmotemporal vein, and across the

rostral aspect of the optic nerve. 118 Just dorsal to the rostrodorsal aspect of the optic nerve, the cerebral ophthalmic artery exits the endocranial cavity and enters the orbit through the cerebral ophthalmic foramen. The cerebral ophthalmic artery is a branch of the rostral cerebral artery (Richards

1967; Baumel 1975, 1993). The cerebral ophthalmic artery then courses rostrodorsally across the ventral aspect of the ophthalmotemporal vein, and then passes medially across the ophthalmic vein (as the latter vein drains into the former). Just past the ophthalmic vein, the artery turns laterally across the vein and anastomoses with the ophthalmotemporal artery

(Richards 1967). The combined artery then passes rostrally away from the dorsal aspect of the ophthalmic vein and courses rostrodorsally across the ventral aspect of the dorsal ramus of the ophthalmotemporal vein. Just rostral to the dorsal aspect of the ophthalmic vein, the artery gives off a long rostroventral branch, the caudodorsal ciliary artery (Hossler and Olson

1984), which forms the dorsal component of the caudodorsal aspect of the ciliary plexus.

Just rostral to the area where the supraorbital vein anastomoses with the dorsal ramus of the ophthalmotemporal vein and forms the nasal vein, the ophthalmotemporal artery courses rostrodorsally across the lateral aspect of the nasal vein to the dorsolateral aspect of the vein. On the dorsolateral aspect of the nasal vein, the ophthalmotemporal artery anastomoses with the supraorbital artery (Richards 1967; Baumel 1975, 1993;

Midtgard 1984a). At the point of the above anastomosis, the ethmoidal artery exits the external olfactory foramen and anastomoses with the ophthalmotemporal + supraorbital artery, and together the three vessels form the nasal artery. The nasal artery then courses rostrally across the dorsolateral aspect of the nasal vein. The ophthalmotemporal artery can travel across the ventral aspect of the ophthalmotemporal and nasal veins, and anastomoses 119 with the supraorbital artery ventral to the nasal vein, even asymmetrically within an individual.

The Lacrimal and Nasal Gland Nerves Within the ophthalmic rete, the lacrimal nerve branches from the lateral aspect of the maxillary nerve and courses dorsally to, and then along, the medial aspect of the profundus vein toward and into the lacrimal gland. Another nerve, which appears to be an early caudal branch of the lacrimal nerve, travels dorsally along the caudal aspect of the profundus vein to the rostroventral aspect of the caudal tail of the nasal gland into which the nerve ramifies.

Orbital Artery The orbital artery courses rostroventral to the oculomotor nerve where the nerve travels to m. rectus medialis. The artery then courses caudodorsally ventral to the oculomotor nerve and across the dorsal aspect of m. rectus ventralis and sends off branches into the plexus located between mm. rectus ventralis, lateralis, and dorsalis. The vessels then courses caudodorsally and sends off a caudal branch that travels caudodorsally between mm. rectus lateralis and dorsalis, and gives off a branch into the plexus between these muscles.

This branch then courses past the caudal aspect of m. rectus lateralis, and then travels dorsally between the caudal aspect of the optic nerve and rostral to the m. rectus dorsalis, and then courses to the ventral aspect of m. rectus dorsalis.

Palpebral Artery Within the temporoorbital canal, the temporoorbital artery sends off a small artery, the palpebral artery, that courses rostrally along the temporoorbital and then profundus arteries into the orbit. The vessel then travels rostrally, across the dorsal aspect of the caudoventrolateral circumorbital membrane, the caudoventromedial aspect of the ventral 120 palpebra, and the ventral aspect of the rostral extension of the lacrimal gland, the latter of which the vessel sends a series of dorsally inclined vessels into. The artery then continues to course across the circumorbital membrane, supplies the medial aspect of the ventral palpebra, and gives off vessels to the rostroventrolateral aspect of the ciliary plexus.

Hyolaryngeal Structures and the Laryngopharynx Rostral to sending off the internal carotid artery, the common carotid artery continues as the external carotid artery, and is ventrally crossed by a caudal branch of the glossopharyngeal nerve, the common trunk of the laryngopharyngealis and descending esophageal nerves, which follows the common carotid artery rostrally, and then follows an arterial branch, the esophagotracheal artery, to the medial aspect of the caudal hyoid. The external carotid artery continues to course rostroventrally with the rostral branch of the glossopharyngeal nerve, the lingual nerve, following along the dorsal aspect of the nerve en route to the lateral hyoidal apparatus.

Caudal Hyoidal Artery Further rostrally, the common carotid artery gives off a rostroventrolateral branch, the caudal hyoidal artery (Richards 1967, for Gallus), that travels toward the ceratobranchial.

The artery then makes a sharp caudally curved turn, and continues to travel caudally in its course across the ceratobranchial and then epibranchial portions of the hyoid, along the ventral aspect of m. branchiomandibularis and through to m. genioglossus, and gives off lateral and medial branches across the muscle’s surface. The vessels terminate at the origin of the cartilaginous portion of the epibranchial. 121 Oromandibular Trunk Rostral to sending off the caudal hyoidal artery, the external carotid artery bifurcates into lateral and medial branches around the mid-caudomedial aspect of m. pterygoideus ventralis at the internal mandibular process (illustrated in Midtgard 1984a) in palaeognaths, galloanserines, and Strix (and perhaps other neoavians). The medial branch, arteria temporomandibularis, is discussed in the section on the infraorbital space. The oromandibular trunk courses ventrally along the medial aspect of m. pterygoideus ventralis toward the dorsal aspect of m. branchiomandibularis.

Just caudal to the caudodorsomedialmost aspect of m. branchiomandibularis, the oromandibular trunk bifurcates into rostral and ventral branches, arteria hyolingualis and the esophagotracheal trunk, respectively.

Esophagotracheal Artery The esophagotracheal trunk travels ventrally across the rostrolateral aspect of the esophagus to the ventromedial aspect of m. branchiomandibularis, with a branch of the glossopharyngeal nerve, and then both artery and nerve bifurcate into rostral and caudal branches (as does the nerve), the descending tracheal and esophageal nerves (Richards 1967;

Baumel 1975, 1993), respectively.

Descending Esophageal Artery The descending esophageal artery courses caudoventrally with the descending esophageal nerve to the ventrolateral aspect of the esophagus. The artery then continues its medial course, passing dorsal to the lingual vein, to the midline of the esophagus, after which the vessel turns caudally and then courses caudally across the ventral surface of the esophagus and gives off a series of ramifying lateral branches across the organ. 122 Descending Tracheal Artery The descending tracheal artery courses rostroventromedially, across the lateral and then ventral aspect of the esophagus (Richards 1967), with the laryngopharyngeal nerve.

Along the ventral esophagus the vessel is ventrally crossed by the rostrolaterally directed hypoglossal nerve, and the vessel then bifurcates into medial and lateral branches, arteriae proper trachealis descendens and hypoglossus, respectively. The hypoglossal artery travels with the hypoglossal nerve to the dorsal aspect of m. ceratobranchialis and the ventral aspect of m. genioglossus. Then hypoglossal nerve and artery then course rostrally between mm. ceratobranchialis and genioglossus toward the urohyal. Rostral to the urohyal, the hypoglossal artery courses and ramifies across the ventral aspect of the tongue.

The proper descending tracheal artery travels rostrodorsomedially to the rostrolateral aspect of the trachea and then bifurcates into rostral and caudal branches. The rostral branch courses rostrally, with the laryngeal nerve, to the caudal aspect of the mons laryngealis and ramifies across and through m. dilator larynges. The caudal branch courses caudally across the dorsolateral aspect of the trachea, sending off a series of ramifying vessels across the external aspect of the trachea in its course.

Hyolingual Artery Along the caudodorsomedialmost aspect of m. branchiomandibularis, the hyolingual artery bifurcates into dorsal and ventral branches, the submandibular and lingual arteries, respectively. The submandibular artery travels rostrodorsally along the dorsal aspect of m. branchiomandibularis and will be further discussed in the section on the palatal region. The lingual artery courses rostrally across the dorsal aspect of m. ceratoglossus, the ventromedial aspect of m. branchiomandibularis, and the lateral aspect of the pharynx. Along the dorsal 123 aspect of m. ceratoglossus, caudal to m. stylohyoideous, the lingual artery bifurcates into

ventral and dorsal branches, the lingual and sublingual arteries, respectively.

The lingual nerve courses medially across the ventrolateral aspect of m.

branchiomandibularis to the ventromedial aspect of the muscle, the dorsal aspect of m.

genioglossus, and the caudomedial aspect of m. stylohyoideous where it meets with the

sublingual artery, and sends off a ventral branch that courses to and then with the proper

lingual artery. The main branch of the lingual nerve then courses rostrally along the

sublingual artery.

Sublingual Artery

The sublingual artery courses with the lingual nerve across the lateral aspect of m. hyoglossus rostralis and sends off a series of ventromedially directed vessels that ramify across and supply the ventral aspect of the muscle. Distally, the artery travels rostroventrally away from the lingual nerve and m. hyoglossus rostralis, then turns and courses rostroventromedially until the vessel meets and anastomoses with the sublingual artery from the opposite side along the mid-ventrocaudal aspect of m. intermandibularis, and forms a single median artery, arteria lingualis media. The median lingual artery then courses rostrally through the intermandibular fascia and sends off a series of lateral vessels that courses across the lateral aspect of the fascia and supplies the ventral aspect of m. intermandibularis. At the rostroventralmost aspect of the mandible, the artery sends off a series of rostroventrally oriented vessels that pass into foramina in the rostroventrolateral aspects of the dentary, near the mandibular symphysis, which supply the rostroventral rhamphotheca and enter into the rostral aspect of the mandibular canal (Baumel 1975). 124 Proper Lingual Artery

The proper lingual artery courses rostroventrolaterally across the lateral and then ventral aspect of the pharynx to the submucosa of the medial pharynx along the rostrolateral aspect of mons laryngealis, into which the artery sends a series of branches and anastomoses with the rostral branch of the descending tracheal artery. The proper lingual artery then courses rostrally, along the ventromedial aspect of m. ceratoglossus, the dorsomedial aspect of m. interceratobranchialis, and the lateral aspect of the larynx, and sends off a rostromedially directed vessel(s), the laryngeal artery (Baumel 1975, 1993), that supplies and ramify within m. constrictor glottidis and the connective tissue associated with the muscle.

More rostral branches of the laryngeal artery supply the area dorsal to the cricoid cartilage, ventral to the arytenoid cartilage, and lateral to the mucosa forming the lateral wall of the laryngeal cavity. Within the lateral aspect of the laryngeal cavity, a shallow fossa is formed in the area between the caudolateral aspect of the arytenoid, ventral to the area of the caudolateral arytenoid, and the caudomedial face of the curved rostroventral aspect of the arytenoid, with the non bony areas formed by mucosa medially and m. constrictor laryngealis laterally. The area of this fossa is particularly vascularized. The connective tissue and some muscle fibers in this area extend caudally past the caudal aspect of the arytenoid cartilages and meet in the midline of the rostrodorsal cricoid to form a mucosa covered mound, through which rostromedial branches of the proper lingual artery ramify and supply. These last vessels send off caudoventral branches that course caudally through the submucosa of the floor of the laryngeal cavity and form a plexus across the floor, including across the laryngeal crest. Further caudally the vessels extend to the floor of the lateral fossa of the 125 laryngeal cavity, then course caudally to and across the internal rostroventral aspect of the trachea, and then travel caudally across this aspect of the trachea.

Distal to sending off the laryngeal artery, the proper lingual artery courses across the lateral aspect of m. cricohyoid dorsalis, then m. hyoglossus obliquus, and finally m. hyoglossus rostralis. Rostral to this area, the sublingual artery diverges rostroventrally away from the lingual nerve, and the nerve continues its rostromedial course to the lateral aspect of the tongue, and, upon reaching it, the nerve meets with the proper lingual artery. The nerve and artery then continue to course rostrally across the lateral aspect of m. hyoglossus rostralis lateralis, and the vessel sends off a dense series of vessels into the tongue musculature which anastomoses with branches from the contralateral proper lingual artery to form an extremely dense plexus within the tongue.

Infraorbital and Antorbital Space

Temporomandibular Trunk The temporomandibular trunk bifurcates into the common maxillomandibular artery and a lateral branch, the rostral auricular artery (Richards 1967; Baumel 1975, 1993).

Rostral Auricular Artery The rostral auricular artery immediately bifurcates into a dorsal branch and a more lateral branch. The dorsal branch(es) ramifies across m. rectus capitis dorsalis along the basisphenoid. The lateral branch passes around the caudal projection of the internal mandibular process, rostral to m. depressor mandibulae pars verticalis, after which the vessel courses dorsal to this muscle. The vessel then travels across the caudal aspect of the quadrate, bends laterally across the rostral aspect of m. depressor mandibulae caudalis, and sends off dorsal and caudal branches into m. depressor mandibulae externus. 126 Common Maxillomandibular Artery The common maxillomandibular artery originates in a position just caudoventral to m. branchiomandibularis. The vessel curves dorsally over the caudal projection of the internal mandibular process, and subsequently curves to the lateral aspect of the internal mandibular process in a position medial to the pterygoid process of the quadrate. The common maxillomandibular artery then curves to the rostral aspect of the rostral quadrate pterygoid process, rostroventral to the tendon of m. pseudotemporalis profundus. In ratites, at the caudal aspect of the adductor muscle mass, the common maxillomandibular artery immediately bifurcates into medial and lateral branches, the pterygoid and proper maxillomandibular arteries, respectively. Whereas, in this same position in galloanserines, the common maxillomandibular artery sends off the mandibular artery and then bifurcates into the pterygoid and jugal arteries (Assenmacher 1953).

Mandibular Artery In Anas and Anser, the common maxillomandibular artery trifurcates at the caudoventralmost aspect of the medial articular condyle of the quadrate. The medialmost vessel, the mandibular artery courses rostroventrally from the caudoventrolateral aspect of m. pterygoideus ventralis as the muscle inserts into the ventral aspect of the internal mandibular process. The mandibular artery is occasionally the first branch of the pterygoid artery. The vessel continues to travel rostroventrally along the medial aspect of the fleshy m. pterygoideus ventralis toward the internal mandibular foramen, and subsequently enters the foramen, with the opportunity to anastomose with the intramandibular artery before or after entering the internal mandibular canal. In galliforms, the mandibular artery branches from the temporomandibular artery as in anseriforms, but is greatly reduced in size, and travels to the foramen as a nearly undetectable, small caliber vessel. 127 In Struthio, the mandibular artery is a much larger vessel that originates from the proper maxillomandibular artery along the rostroventrolateral aspect of the lateral condyle of

the quadrate, medial to the jugal-maxilla sutural contact. The mandibular artery courses

rostroventrally, across a broad groove along the rostrolateral aspect of the articular bone

medial to the bone’s contact with the prearticular. In this course, the mandibular nerve

travels across the caudolateral aspect of the tendon of m. pterygoideus ventralis as the

tendon inserts into the internal mandibular process. Rostral to the groove, the artery courses

rostrally across the medial aspect of the mandible towards the internal mandibular foramen

and subsequently enters into it. In ratites, the temporal artery gives little contribution to the

internal mandibular canal. The branching pattern and size of the mandibular artery in ratites

is quite dissimilar to the galloanseriform condition, but is very similar to crocodilians. In

galloanserines, the quadrate is twisted caudolaterally in comparison to the ratite quadrate,

with the result that the medial condyle is actually closer to the internal mandibular foramen

than is the lateral condyle, which is the reverse of the ratite condition. It is possible that the

change in the branching pattern of the mandibular artery from the common

maxillomandibular artery is a result in the quadrate’s positional change. The ratite proper

maxillomandibular artery refers to the common branch of the jugal and mandibular arteries.

Jugal Artery In Anas, the jugal artery turns and curves rostrolaterally around the dorsolateral

aspect of m. pterygoideus ventralis, then across AMEPR, and finally AMEPC. Along its

course, the vessel sends off dorsal, medial, and rostral branches into each of these muscles

and travels close to the rostroventral aspect of the pterygoid process of the quadrate. Just

lateral to the pterygoid process of the quadrate, the muscle and tendon of AME medialis 128 crosses over the rostrolateral aspect of the jugal artery, after which the vessel curves rostrolaterally around the lateral aspect of AMEPC and gives off dorsal branches that ramify into AMEPC, AMEPR, and AM caudalis. The artery then courses laterally across the rostroventral aspect of the mandibular process of the quadrate toward the medial aspect of the quadrate-jugal sutural contact. In this course, the artery travels dorsal to the rostral aspect of the articular condyles and quadratoarticular joint capsule, and across the caudoventral aspect of AME medialis. Upon reaching the quadrate-jugal sutural contact, the jugal artery curves rostrodorsally along the medial aspect of the joint to the dorsomedial aspect of the jugal and the lateral aspect of AME medialis, and then courses rostrally across the medial aspect of this last muscle. The vessel then continues to course rostrally across

AMEPC, dorsomedially paralleling the jugal bar. The jugal artery gives off large branches that ramify across the superficial surface of AMEPC, at a point where the artery, jugal bone, and adductor musculature are laterally crossed over by the lacrimomandibular ligament. At the point the artery, jugal, and adductor musculature are laterally crossed over by the lacrimomandibular ligament, the jugal artery gives off a ventral branch that passes medial to the jugal, descends ventrally, and ramifies across and into AM caudalis. The jugal artery then continues its rostral course, deep to and then rostral to the lacrimomandibular ligament, and then sends branches to and across m. adductor mandibulae superficialis, after which the vessel curves rostrodorsally along the rostral aspect of the superficialis component of

AMEPR. At the corner of the mouth (marked by the rostralmost aspect of the adductor musculature), rostral to the superficialis component of AMEPR and slightly caudal to the lacrimojugal ligament, the vessel splits along the surface of the skin at the corner of the 129 mouth (the skin extends across the antorbital sinus and caudally to the lacrimojugal ligament)

into dorsal and ventral branches.

The dorsal branch of the jugal artery, the facial artery, extends rostrodorsally along the lateral aspect of the rostral lacrimal bone, and gives off several rostral branches that ramify across the skin covering the external antorbital fenestra, and gives off dorsal branches that ramify dorsally, rostrally, and caudally across the surface of the nasolacrimal duct.

Further dorsal, the facial artery sends off caudally directed vessels to the ventral palpebra, then the dorsal palpebra, and terminates as the dorsally directed frontal artery which courses rostrodorsally along the dorsolateral aspect of the lacrimal bone, then across the rostral aspect of a caudodorsolateral process of the lacrimal, and finally to the scalp into which the vessel ramifies across the dermis (Richards 1967; Baumel 1975, 1993; Midtgard 1984a). In

some galliforms (e.g., Meleagris), the frontal artery passes to the scalp by passing through a laterally facing notch between the rostrodorsolateral lacrimal bone and the caudodorsolateral nasal bone.

The ventral branch of the jugal artery is oriented rostroventral to the jugal at about

the level of the lacrimojugal ligament, and continues to travel rostrally across the dorsal

aspect of the jugal to the rostral aspect of the antorbital cavity, where it then ramifies across

the caudal rhamphotheca near the maxillary-jugal junction. Just caudal to this area, the

vessel gives off a rostromedial branch that curves over the dorsal surface of the rostral

pterygoid periosteum, across the ventral aspect of the antorbital sinus, where it sends off

small, thin branches across the bone which then course rostrally through the foramen for the

lateral branch of the dorsal alveolar nerve. The arterial branches continue to course through

the canal for the lateral branch of the dorsal alveolar nerve. These branches supply the 130 caudal maxilla, and ultimately exit laterally through a series of small neurovascular foramina in the caudoventrolateral aspect of the maxillary contribution to the rhamphotheca, where they anastomose with branches of the dorsal lateral rhamphothecal artery. This last artery is potentially homologous with the dorsal alveolar artery of ratites.

Pterygoid Artery The pterygoid artery travels rostrodorsally across the ventromedialmost aspect of the pterygoid, and gives off small vessels that ramify ventrally across the pterygoid to supply m. pterygoideus ventralis and to more densely supply the body of m. pterygoideus dorsalis. The pterygoid artery then passes to the lateral aspect of the pterygoid on the rostromedial aspect of m. pseudotemporalis profundus where it is crossed by the mandibular nerve branch to m. pterygoideus dorsalis, after which the vessel passes over the origin of the caudal aspect of m. dorsal pterygoideus along the ventrolateral aspect of the palatine bone. The artery gives off a long rostrolateral branch into m. pterygoideus dorsalis which then ramifies within the muscle body. In this vicinity, the artery is slightly parallel to the large facial vein that drains the facial region, and the artery subsequently becomes oriented as a dorsally inclined arterial trunk that bifurcates into caudodorsal and rostral branches.

The caudodorsal branch passes along the tendon of m. protractor pterygoideus, and early in its course, the artery gives off a rostrodorsal branch across the rostrolateral aspect of the muscle body. The main continuation of the artery branches across the caudal aspect of m. protractor pterygoideus and sends small nutrient vessels into the muscle body.

The rostral branch of the pterygoid artery breaks up into a series of long, thin, closely spaced arteries that parallel each other and travel along the ventral, lateral, and medial surfaces of the maxillary vein, and provides vessels that travel along the dorsal aspect of the 131 vein. This creates a unique vascular arrangement, in that the vein primarily responsible for draining the nasal, oral, and orbital region is completely enclosed by a dense array of arteries en route to the nasal and oral cavities, in essence forming a perivenous vascular physiological device. This has been described in Gallus as the pterygoid plexus (Baumel 1975, 1993).

The sphenomaxillary artery enters the infraorbital space by passing dorsomedial to the basipterygoid process, running along a shallow groove in the ventrolateral surface of the process. Proximal in this course, the artery is laterally crossed by the tendon of m. protractor pterygoideus.

Rostral to the basisphenoid-pterygoid articular capsule and dorsal to m. pterygoideus dorsalis, the maxillary vein receives a long vertical vein, the ophthalmic vein. The ophthalmic vein first drains ventrally from the eyeball across the rostral portion of m. protractor pterygoideus and then across the rostrodorsal aspect of the articular capsule before emptying into the facial vein. The dorsal branch of the palatine ramus of the facial nerve, which travels on the dorsomedial aspect of the sphenomaxillary artery, travels onto the ventral component of the ophthalmic vein and courses dorsally along the medial aspect of the vein towards the eyeball. In its rostral course, the dorsal ramus of the artery of the pterygoid canal passes medial to the vein. Just rostral to the ophthalmic vein, the artery anastomoses with dorsal and lateral plexiform arteries derived from the pterygoid artery

(Baumel 1975), and contributes to the peri-venous arterial plexus.

A large caudoventrally directed vein, the orbitonasal vein, enters the orbit medial to the dorsalmost aspect of the thin os ectethmoidale and lateral to a thin but tough membrane in the rostral orbit. The vein runs along the caudal aspect of the bone in its descent toward the maxillary vein. In its course, the orbitonasal vein receives a series of vessels from the 132 dorsomedial and then the ventromedial aspects of the caudal concha. The vein passes caudodorsally over the caudodorsal aspect of m. pterygoideus dorsalis before draining into the maxillary vein. The arterial plexus formed by branches of the sphenopalatine and pterygoid arteries travels as a dense plexus along this vein toward the caudal concha. The arteries travel rostrally, paralleling the veins in their caudal course, along the dorsal vomer, between the vomer and the interorbital septum, and then between the dorsal aspect of the premaxillary process of the maxilla and the internasal septum. More dorsal vessels travel along the internasal and interorbital septa to the caudal concha and to the rostral aspect of the ectethmoid. The septal and vomerine vessels anastomose in a plexus across the septal wall.

The sphenopalatine and pterygoid arterial plexus splits around the ophthalmic vein and anastomose rostral to the vein, on the dorsal aspect of the maxillary vein, to form more prominent arteries that pass over the lateral aspect of m. pterygoideus dorsalis and which surround a large vein draining from the muscle. The maxillary vein then curves along the rostral aspect of m. pterygoideus dorsalis and caudal to the lateral palatine fossa. The arteries from the arterial plexus in this region send branches to the ventral aspect of the maxillary nerve where the nerve bends under the ectethmoid, after which the vessels spread both rostrally and caudally across the maxillary nerve. The pterygoid artery(ies) passes through a bony aperture on the dorsal palatine bone which leads to a rostrally oriented groove in the palatine. The arteries, which surround a large vein, the palatomaxillary vein, that ultimately drains into the maxillary vein, travel rostrally along the floor of the groove, dorsal to the palatine periosteum and ventral to the maxillary nerve. An incomplete maxillary neurovascular canal is formed by the caudal concha dorsally, the palatine groove 133 ventrally, a thin, clear, but strong tissue that extends from the lateral caudal concha to the dorsal border of the palatine border lateral to the palatine groove, and a thin membrane that stretches from the medial aspect of the palatine groove to the ectethmoid.

In its ventral descent, the antorbital arterial plexus completely encircles the maxillary vein forming a loop around the vein and anastomoses, on the medial aspect of the vein, and on the rostral aspect of m pterygoideus dorsalis, to form a single large caliber artery. This artery then descends, first past the pterygoid, then over the medial aspect of the oropharyngeal mucosa, and finally anastomoses with the submandibular artery.

Before passing caudally through the arterial loop, dorsal to the tendon of m. pterygoideus rostralis and medial to the rictal submucosa, the maxillary vein receives a caudoventrally directed vein, the palatine vein, which drains the lateral and median palatine arteries, and a caudodorsally directed vein, the rictal vein, that drains the rich venous plexus within the submucosa of the rostral margin of the rictus and the external maxillary and mandibular veins.

Palatomaxillary and Dorsal Alveolar Arteries Early in their course the palatomaxillary branch of the maxillary nerve and the palatomaxillary artery both divide into lateral and medial branches. The medial branch follows the dorsal palatine groove medially to a caudal foramen in the dorsal palatine. This foramen is occasionally incompletely closed (usually the lateral aspect), or occurs as just a large gap in the palatine. The foramen leads to a bony canal formed exclusively by the palatine. The lateral branch completely occupies the dorsum of the rostrolateral palatine, and the lateral ridge of the dorsal palatine groove separates the lateral and medial branches. 134 At the rostroventralmost aspect of the antorbital fossa, the palatomaxillary artery and nerve divide again into lateral and medial components, the dorsal alveolar and palatine neurovascular bundles, respectively. The palatine nerve is larger and passes through an aperture formed by the maxilla laterally, the premaxillary process of the maxilla medially and dorsally, and the rostromedial palatine ventrally. This nerve grooves the ventral aspect of the premaxillary process of the maxilla. The palatine nerve then passes through a short canal formed by the above bony structures, and opens into a grooved channel on the caudal aspect of the ventrolateral premaxilla, rostromedial to the premaxillary process of the maxilla.

Vessels passing along the above nerves supply and drain the dense plexus in the caudal concha through a series of dorsally directed branches.

The dorsal alveolar neurovascular bundle enters a foramen in the ventrolateral maxilla, dorsal to the rostrolateral palatine, within the rostralmost aspect of the antorbital cavity. The neurovascular bundle passes through a series of channels in the maxilla and divides into two major branches, a caudal branch that exits through caudolateral maxillary foramina (or a single large foramen), and a rostral branch that exits through rostrolateral maxillary foramina. The latter vessels, upon exiting, become rostrally inclined and course across the dorsal rhamphotheca, deeply grooving the maxilla.

In Anser, veins drain from the lateral nasal canal medially across the bony bridge between the lateral and medial nasal canals. Veins drain from the medial nasal canal into a vein dorsal to the medial nasal foramen. This vein receives blood draining from the skin that empties between the lateral frontal process and the frontal (a notch dorsal to the ectethmoid). The vein further receives blood from the fossa located medial to the ectethmoid which leads into the olfactory groove. The venous system drains into the 135 olfactory plexus or into the ventrally inclined orbitonasal vein that passes along the rostral aspect of a vertical groove located in the interorbital septum caudal to the ectethmoid, and which originates from the rostroventral olfactory groove and travels ventrally to the ventral interorbital septum at the septum’s junction with the palate (illustrated in Midtgard 1984a).

The ventral aspect of the suborbital sinus passes into the lateral nasal canal and into the fossa medial to the ectethmoid.

In Anser and Anas, a large dorsolateral foramen in the maxilla contains the rostral diverticulum of the antorbital sinus. In both species, the vertical, rostral aspect of the suborbital diverticulum is medial to the lacrimal and mainly caudal to the ectethmoid

(Witmer 1995b). The lateral nasal canal is situated between the lacrimal and the ectethmoid

(Baumel and Witmer 1993).

The lateral aspect of the antorbital sinus rests on the dorsal aspect of the jugal bar.

Rostral to the lacrimal, the antorbital sinus descends, through the suborbital palatine diverticula, ventrally between and beyond the palatine and jugal, and partially fills the infundibular space. The antorbital sinus is compressed against the most lateral aspect of the palatine and ascends above it, and forms the lateral border of the maxillary neurovascular canal (Witmer 1995b).

In domestic ducks, the vertical suborbital sinus plexus is situated between the lateral aspect of the interorbital septum and the medial aspect of the lacrimal, caudal to the ectethmoid, and rostral to the eyeball. The suborbital diverticulum is situated in an area ventral to the ventral periorbitum, and the plexus associated with the diverticulum has a dense anastomotic relationship with the ventral periorbital plexus, which receives a dense 136 array of veins from the vertical suborbital sinus plexus, and drains caudally into the ophthalmic rete.

In Gallus, there is a similar connection between the antorbital plexus, the suborbital plexus, and the ophthalmic rete. The plexus is vertically oriented just rostral to the eyeball, and receives vessels that pass caudally through the notch between the lacrimal and frontal bones. The antorbital plexus completely covers the sinus, and drains, through several vessels, into the vertical aspect of the suborbital plexus, and more ventrally into the caudal, horizontal, aspect of the suborbital plexus. The lateral nasal vein courses caudally, between the lacrimal and ectethmoid, and drains across and receives the medial nasal vein, and the vein from the notch. This vein directly receives a vein that passes through a foramen in the dorsolateral lacrimal, which itself drains the comb. The vein then drains into the supraorbital vein and the orbitonasal vein which drains ventrally along the caudal aspect of the ectethmoid. The orbitonasal vein drains caudoventrally along the contours of the orbital septum into the nictitating vein and the periorbital plexus. The rostral part of the maxillary vein receives the palatine vein and the rictal vein, and more caudally receives the dorsal alveolar vein. Near the area of the palatine-pterygoid sutural junction, the maxillary vein drains the nictitating vein.

Brief survey of the Infraorbital, Antorbital, and Palatal Vasculature in Ratites The anatomy of the infraorbital, dorsal alveolar, and palatal vasculature in Struthio and Dromaius is evolutionarily important in that the structure and pattern of the vasculature is more similar to that found in Crocodylia than to the neognath condition.

The maxillary artery sends off a rostroventrally oriented vessel to the infraorbital mucosa, which then courses rostrally across the mucosa and then across the mucosal lining 137 the ventrolateralmost aspect of the maxilla, and finally across the mucosal lining the ventrolateral aspect of the premaxilla and sends off branches that enter into the caudoventral premaxillary foramina in this region. The continuing branch of the maxillary artery, the palatomaxillary artery, courses rostrally and bifurcates near the jugal-maxilla sutural contact, just caudal to the caudoventralmost aspect of the lacrimal in the area between the caudal aspects of the jugal and palatine processes of the maxilla, into lateral and medial vessels, the arteria alveolofacialis dorsalis and palatine arteries, respectively. The dorsal alveolofacial artery travels laterally through a groove across the caudoventral aspect of the lacrimal toward the medial aspect of the lacrimal-maxilla suture. Near the caudoventrolateral aspect of the lacrimal, the alveolofacial artery bifurcates into dorsal and ventral branches, the facial and dorsal alveolar arteries, respectively.

The facial artery curves and travels rostrodorsally around the ventrolateral aspect of the lacrimal, and then courses rostrodorsally across the lateral aspect of the lacrimal, sending off rostrally directed branches to the lateral aspect of the antorbital sinus. The artery then continues to course dorsally, sending off caudal branches to the ventral and then dorsal palpebrae, past the external antorbital fenestra to the dorsolateral aspect of the lacrimal, and finally travels medially to the dorsal aspect of the lacrimal and ramifies through the dermis of the scalp.

The dorsal alveolar artery and nerve course rostroventrolaterally to the caudodorsolateral aspect of the jugal process of the maxilla, and then travel rostrally across the dorsolateral aspect of the jugal process of the maxilla toward the dorsal alveolar canal in the caudodorsolateral aspect of the main body of the maxillary bone. The dorsal alveolar neurovascular bundle then courses into the dorsal alveolar canal and then rostrally through 138 it. Within the caudolateral aspect of the dorsal alveolar canal is a separate longitudinally oriented nutrient canal, the neurovascular bundle sends off early lateral branches that course rostrally through the nutrient canal which send off a series of laterally directed branches that pass to the external aspect of the maxilla through a series of small nutrient foramina on the dorsolateral surface of the main body of the maxilla. Within the caudal aspect of the nutrient canal, the neurovascular bundle sends off a caudoventrally directed branch that passes through a canal and exits into the caudoventral aspect of the main body of the maxilla; the vessels running along the ventrolateral aspect of the maxilla can pass into the nutrient canal through this foramen and anastomose with the nutrient vessels. Medial to the nutrient canal, within the dorsal alveolar canal, is another longitudinally oriented canal in which medial branches of the neurovascular bundle course rostroventrally through the canal and then out through a foramen opening into the rostroventral aspect of the main body of the maxilla, and then anastomose with the ventral maxillary vessels. The chambers in the dorsal alveolar canal medial to the two neurovascular canals are actually pneumatic and contain the rostral maxillary diverticula of the antorbital sinus (illustrated in Witmer 1990).

The palatine artery courses rostromedially through the mucosa stretched across the area between the maxillary process of the palatine and the jugal process of the maxilla. In the center of the caudal aspect of this area, the palatine artery bifurcates into lateral and ventral branches, the lateral and medial palatine arteries, respectively. The lateral palatine artery courses rostrally across the mucosa of the suborbital fenestra to the mid-caudalmost aspect of the main body of the maxilla, and then courses rostroventral to this aspect of the maxilla, and continues its course across the main body and premaxillary process of the maxilla. It is this vessel that anastomoses with the ventral branches of the dorsal alveolar 139 artery. Rostrally, these vessels pass through foramina along the ventral aspect of the maxillary process of the premaxilla and the main body of the premaxilla, which open to the rostrodorsal aspect of the rhamphotheca through foramina in the rostrodorsal aspect of the premaxilla.

The medial palatine artery continues to course rostromedially and courses across the rostrodorsal aspect of the maxillary process of the palatine and then across the palatal submucosa medial to the palatine bone. The submucosa that the palatine artery courses across lines the dorsal aspect of the thick mucosa that spans the area caudal to the main body of the maxilla and between the jugal processes of the maxilla, and is caudolaterally confluent with the choanal torus. The area between the jugal process of the maxilla, the main body of the maxilla, and the maxillary process of the palatine is the rostral aspect of the suborbital fenestra. As in all neornithines, Struthio lacks an ectopterygoid, which results in the confluence of the suborbital and subtemporal fenestrae. The lateral palatine-pterygoid suture would be the suborbital fenestra’s caudomedial boundary. This entire area is just ventral to the ventral aspect of the suborbital diverticulum. The medial palatine artery then continues its rostromedial course, traveling along the caudal aspect of the vomerine process of the maxilla, toward the ventrolateral aspect of the vomer, and early on sends off a rostrolaterally directed vessel that anastomoses with a vascular plexus on the ventral aspect of the main body of the maxilla. In its course across the vomerine process of the maxilla, the medial palatine artery anastomoses with a dense array of vessels derived from the submandibular artery that courses rostromedially toward the vomerine process of the maxilla, through the submucosa of the choanal torus and of the lateral suborbital fenestra.

The medial palatine artery then courses to the mid-caudal aspect of the vomer and 140 anastomoses with the medial palatine artery from the opposite side to form a single median palatine artery.

The median palatine artery courses rostrally across the mid aspect of the soft palate, dorsal to the median palatine nerve (which forms a longitudinal ridge, as in Anas) and sends off a series of lateral vessels that travel to anastomose with the plexus along the ventral aspect of the maxilla. In an area parallel to the rostrolateral premaxilla-maxilla sutural contact, the median palatine artery bifurcates into right and left branches. These branches course rostrodorsally to the dorsolateral aspect of the premaxilla, and the lateral aspect of the nasal vestibule, and then travel rostrally across the dorsal aspect of the premaxilla and immediately anastomose with the medial nasal artery, and further rostral, with the terminal component of the rostroventrally descending lateral nasal artery. The vessel resulting from this anastomosis then enters into a caudally open, ventrolaterally oriented foramen in the caudal face of the premaxilla facing into the rostral aspect of the nasal vestibule, and before entering the foramen, sends off branches to pass into a more dorsomedial foramen and a third foramen dorsomedial to the second. Each of these premaxillary arteries then course rostrally through the premaxillary canals which will pass to the external rostroventral and rostrodorsal aspects of the rhamphotheca via a series of rostroventral, and rostrodorsal foramina, respectively, and will further anastomose with branches of the ventrolateral maxillary arteries.

Oropharynx

Basic Anatomy of the Caudal Oropharynx The medial palatal torus is rostrally attached to the entire ventral aspect of the palatine, more caudally along the medial aspect of the foot of the pterygoid, and finally along 141 the medial aspect of the quadrate process of the pterygoid. Caudal to the infundibulum the

medial palatal torus of each side meets to form a single wide median caudally directed torus.

This caudal torus is oriented ventral to m. longus colli, and turns into the rostral pharynx.

The infundibulum is ventrally situated in the space between the basipterygoid processes and

becomes medially continuous with the medial palatal torus along its attachment to the foot

of the pterygoid. In the rostralmost aspect of the infundibulum is a small bulbous structure,

with a ventrally open ostium, which is continuous with a mucosal fold that passes

caudodorsally between the two sides of the infundibulum. The mucosa of the

caudolateralmost aspects of the infundibulum form the rostral aspects of the

pharyngotympanic tubes.

The vomerine mucosa originates on the caudal aspect of the vomer, ventral to the

dorsal vomerine ridge, and attaches ventrally along a caudoventrally directed ridge on the vomerine process of the palatine and has a strong insertion into a medial ridge along the medial pterygoid process of the palatine. Caudal to the above insertion, the vomerine mucosa becomes continuous with the medial palatine torus which inserts in this region along the medial aspect of the palatopterygoid joint. The area delineated by the mucosal insertion on the caudalmost vomer, the mucosal insertion into the medial ridge along the medial pterygoid process of the palatine, and the caudalmost aspect of the infundibulum, forms a large bulbous structure. A median ridge runs caudally along the ventral aspect of the vomerine bulb and then bifurcates into caudolaterally directed ridges which end in the medial palatal torus, lateral to the rostral aspect of the infundibulum. The above mentioned bulb, an apparent outpocketing of the median pharyngotympanic tissue, is partially enclosed by a notch formed by the rostral meeting of the two infundibular crests. 142 On each ventrolateral aspect of the paraphenoid rostrum is a crest that projects ventrally from the bone and extend caudolaterally, from a common point between the caudomedial aspects of the basipterygoid processes, to an area just rostral to the ostium for the common pharyngotympanic tube (a single median crest continues from the rostral convergence of these crest and extends rostrally across the parabasisphenoid rostrum). The walls of the infundibular orifice, the antrum of the pharyngotympanic tube, extend dorsally and insert into these crests, which will be referred to as the infundibular crests. In Anas, a large foramen, the orbital foramen, is located just lateral to the median aspect of the infundibular crest. At its caudal extent, the infundibular crest curves medially toward the ostium for the common pharyngotympanic tube, and a second, smaller foramen, the caudal sphenoid foramen, is located caudolateral to this aspect of the crest.

The horny choanal torus inserts along the medial aspect of the palatine and extends slightly into the bony secondary choanae. The choanal torus then turns ventrolaterally upon itself and extends laterally, ventral to the palatine bone, after which the torus becomes ventrolaterally continuous with the mucosa of the corner of the mouth, which itself is caudally continuous with the pharyngeal mucosa. The choanal torus is rostrolaterally continuous with the rictus. Tendinous fibers of m. pterygoideus ventralis insert along the mid- and caudal palatine pars choanalis periosteum; as a result, the rostral body of m. pterygoideus ventralis is partly enclosed by the submucosa of the choanal torus ventrally and the palatine dorsally.

Sphenopalatine Artery As mentioned above, the dorsal facial nerve divides into a caudal ramus, the hyomandibular nerve, and a rostral ramus, the palatine ramus. Figure 6C depicts the major 143 arteries of the orophayrnx and palate. The palatine ramus of the dorsal facial nerve further divides into dorsal and ventral branches. Both rami of the palatine nerve exit the sphenomaxillary canal through the rostral orbital foramen with the sphenomaxillary artery, and split around the artery. The dorsal branch of the palatine ramus follows closely along the lateral aspect of the sphenomaxillary artery, which courses rostrodorsally away from the parabasisphenoid, ventral to the articular capsule of the pterygobasipterygoid articulation, and laterally through the notch defined by the dorsal aspect of the joint capsule and the dorsal aspect of the pterygoid bone. The ventral ramus of the palatine nerve passes along the lateral aspect of the infundibular crest and the laterodorsal aspect of the antrum of the pharyngotympanic tube, and subsequently passes between the antrum and the joint capsule into a bulbous space caudal to the choana, and then travels with the sphenopalatine artery.

The sphenopalatine artery passes through the caudal sphenoid foramen. The first branch of this vessel curves caudomedially over m. longus colli. The sphenopalatine artery then twists rostroventrally across the laterodorsal antrum and then bifurcates, in a region medial to the foot of the pterygoid, into lateral and medial branches.

The medial branch of the sphenopalatine artery courses rostromedially and again bifurcates into lateral and medial rami. The medial ramus gives off a series of medial branches over the body of m. pterygoideus ventralis; subsequently, the vessel passes through m. pterygoideus ventralis, then passes ventral to and passes across the muscle, and ultimately spreads caudolaterally across the submucosa of the caudal palatal torus. The lateral ramus sends off a branch that travels laterally toward the lateral aspect of the pterygobasipterygoid joint capsule, and then runs rostroventrally across the joint capsule to an area between the capsule and the pterygoid bone. The vessel then travels medially toward the tendon of m. 144 pterygoideus ventralis (which inserts into the caudomedial pterygoid process), passes

ventrally under the tendon, courses rostromedially beyond the tendon, and then

anastomoses into a dense vascular plexus situated between the submucosa of the choanal

torus and the periosteum of the palatine bone.

The sphenomaxillary artery courses rostrally between the joint capsule and the

dorsolateral aspect of the antrum, and sends vessels into the space within the vomerine bulb.

The continuation of the sphenomaxillary artery closely follows the course of the dorsal

branch of the palatine ramus of the dorsal facial nerve. The sphenomaxillary artery then

bends around the rostrodorsalmost aspect of the pterygobasipterygoid joint capsule, and

passes laterally into the infraorbital space, through the fenestra formed by the rostrodorsal

pterygoid and the caudoventral mesethmoid. The nerve and artery then pass rostrolaterally

across the ventrolateral aspect of the vomerine process of the pterygoid and dorsal to the

dorsolateral pterygoid process of the palatine. Early in its infraorbital course, the dorsal

branch of the palatine ramus and the sphenomaxillary artery travel first medial to and then dorsal to the maxillary vein and its associated arterial plexus as the vein crosses the lateral palatopterygoid joint. The nerve then courses rostrodorsally toward the dorsal aspect of the vomer along the dorsal aspect of the caudodorsal palatine and along the ventral aspect of the vomerine process of the pterygoid, passing laterally across the orbital ligament which inserts into the palatopterygoid joint. The nerve then passes along the dorsal aspect of the vomerine process of the palatine and reaches the dorsalmost aspect of the dorsal ridge of the vomer. The nerve and vessel then pass rostrally along this dorsal ridge toward the nasal cavity. 145 Submandibular Artery Early in its course, the submandibular artery gives off a branch(es) to m.

branchiomandibularis that courses rostral and parallel to the glossopharyngeal nerve. The

first large caliber branch of the submandibular artery passes dorsally and ramifies along the

rostrolateral aspects of the choanal torus and vestibular bulb. The next branch of the

submandibular artery passes medially to the caudal aspect of m. pterygoideus ventralis. The continuation of the submandibular artery passes ventrolateral to, and then laterally parallels, m. pterygoideus ventralis, after which the artery gives off a series of small rostroventral

branches to the ventral aspect of the rictus (Baumel 1975). The vessel then passes over the

tendon of m. pterygoideus ventralis to lie in a position dorsal and parallel to the tendon, after

which the vessel splits into rostral and dorsal branches, arteriae rictalis and pterygopalatinas,

respectively.

Rictal Artery The rictal artery immediately splits into ventral and dorsal branches (Midtgard

1984a). The dorsal branch curves sigmoidally, first across the caudal process of the maxilla, and then along the caudal process of the nasal bone. Throughout its course the artery gives off a series of caudally directed arteries that ramify across the antorbital sinus. The dorsal rictal artery divides into several branches at the rostrodorsal aspect of the caudal maxillary and frontal processes creating a dense arterial plexus along the caudal rhamphotheca. Early in its course the dorsal rictal artery gives off a rostral branch that courses across the caudoventral maxilla, ramifies across this aspect of the rhamphotheca, and sends vessels into the lateral maxillary nutrient foramina which anastomose with branches of the dorsal alveolar artery. In its more dorsal course, the dorsal rictal artery sends off vessels that pass 146 over the caudodorsal aspect of the premaxillary process of the maxilla and which then anastomose into the plexus of the middle concha.

The ventral rictal artery becomes intimately associated with a branch of the mandibular nerve, the nerve to the angle of the mouth. In its early course, by which the nerve innervates the trigeminal musculature, the mandibular nerve steeply travels rostroventrally, in close association with the internal mandibular artery, first medial to

AMEPC, and then medial to AMEPR, eventually entering with the artery a large foramen in the medial aspect of the coronoid bone which opens into the internal mandibular neurovascular canal. Early in its course, the internal mandibular nerve gives off the external mandibular branch which exits to the external aspect of the mandible through a foramen located in the coronoid bone, rostral to the process for the insertion of AMEPC, and medial to the tendon of the superficialis component of AMEPR. The nerve courses rostrally across the latter muscle, across the ventral coronoid bone, dorsal to the caudal process of the dentary. The nerve comes into close contact with the ventral rictal artery at the angle of the mandible, along the rostroventral aspect of the coronoid process. The nerve and artery proceed rostrally through a deep groove in the dentary. In its course the rictal nerve gives off long rostrodorsal nerves into the ventral lamellae, and along the ventral rictal artery gives off small, dense anastomotic branches across the lateral aspect of the mandible, many of which anastomose dorsally with the arteries supplying the ventral lamellae.

Median Palatine Artery The dorsal branch of the submandibular artery, the pterygopalatine artery, travels medially toward the medial mucosal wall of the antorbital cavity and passes ventral to the antorbital sinus in its course. This branch then passes over the origin of m. pterygoideus 147 dorsalis, and at this point is crossed by the maxillary vein. The pterygopalatine artery courses rostral to the body of m. dorsalis pterygoideus and the lateral pneumatic fossa of the palatine bone where it anastomoses with the pterygoid artery (Baumel 1975, 1993) to form the common palatine artery. The common palatine artery courses rostrodorsally across the mucosa of the corner of the mouth in the rostromedial antorbital cavity, and subsequently passes ventral to the palatine bone, just caudal to the notch in the rostral antorbital fossa formed laterally by the caudal process of the maxilla and medially the lateral aspect of the palatine.

The common palatine artery travels rostrally along the ventrolateral aspect of the palatine pars choana. Caudal to the rostral palatine notch (the rostral border of which is formed by the maxilla) the vessel splits into lateral and medial rami. The lateral ramus passes along the ventral aspect of the palatine and then descends ventrally to the dorsal margin of the caudal lamellae. Early in its course the lateral ramus gives off a dense array of anastomosing vessels, which pass medially into the arterial plexus within the submucosa of the torus palatina. The lateral ramus then courses rostrally along the dorsal margin of the dorsal lamellae and gives off a series of ventrolateral branches that supply the lamellae. The medial ramus, the medial palatine artery, curves rostromedially to the ventral palatine crest, and subsequently courses ventrally across the crest, along the ventromedial aspect of the choanal torus. Early in its course, the medial palatine artery gives off caudal vessels that anastomose into a dense vascular plexus (along with branches of the palatine ramus of the artery of the pterygoid canal) located medial to the bony secondary choanae, dorsal and lateral to the submucosa of the choanal torus and ventral to the palatine periosteum. The choanal plexus is especially dense in the region just medial to the choanal opening. 148 The medial palatine artery then curves rostromedially across the premaxillary process of the maxilla, rostral to the caudal aspect of this bony region, to the suture between the two premaxillary processes, and anastomoses with the medial palatine artery from the opposite side to form a single median palatine artery (Baumel, 1975, 1995; Midtgard 1984a). The median palatine artery then travels rostrally through the dermis, which is situated ventral to the periosteum and dorsal to the horny rhamphotheca which covers the suture between the two premaxillary processes of the maxillae (completely fused in the adult, toward the large, ventral aspect of the palatine fenestra).

The palatine fenestra is situated within the median aspect of the rostral bony palate, between the palatine processes of the premaxillary bones. The dorsal aspect of the palatine fenestra opens into the median aspect of the nasal vestibule. The ventral (palatal) aspect of the palatine fenestra is covered by rhamphotheca, whereas the dorsal (nasal) aspect of the fenestra is covered by nasal mucosa, and the median palatine artery traverses the fenestra, traveling rostrally through the submucosa between the above mentioned rhamphothecal and mucosal tissues. The rhamphothecal tissue ventrally lining the median palatine fenestra, and extending caudolaterally from the fenestra toward the caudalmost bony palate until it reaches the tomial crest, is softer and paler in color than the rhamphothecal tissue covering the rest of the palate. The rhamphothecal tissue just ventral to the median palatine artery, throughout much of the course of the vessel, forms a strong, rostrocaudally oriented ridge that dorsally and laterally encloses, and is likely formed by, the median palatine artery.

In the area of the palatine fenestra, the rhamphothecal ridge bears a row of knob-like protuberances. In its course across the palatine fenestra, the median palatine artery gives off a series of lateral vessels that travel toward the lateral palatine plexus (Midtgard 1984a), into 149 which they anastomose. Near the caudal aspect of the palatine fenestra, the median palatine artery gives off laterodorsally directed right and left vestibular branches. Near the lateralmost aspects of the palatine foramen, these vestibular arteries pass through the nasal mucosa and into the nasal vestibule where they anastomose with the medial nasal arteries

(Baumel 1975, 1993; Midtgard 1984a) along the caudolateral aspect of the maxillary process of the premaxilla and parallel to the caudalmost maxilla-premaxilla sutural contact. The median palatine-medial nasal arterial anastomosis will be further discussed in the section on the nasal cavity.

At the rostralmost aspect of the palatine fenestra, large ventral branches of the medial nasal nerves pass rostroventrally through the nasal mucosa into the submucosa, and turn medially toward one another until they lie in close apposition. Rostral to the palatine fenestra, the two nerves course rostrally and form a wide, deep, rostrocaudally oriented groove across the median rostral bony palate, along and lateral to the suture between the right and left palatal processes of the premaxillae. The median palatine artery, rostral to the palatine fenestra, is situated in a position just ventral to the medial aspects of the two palatal branches of the medial nasal nerves. In their rostral course, the median palatine artery and the two palatal branches of the medial nasal nerve give off a series of lateral branches across the rostral bony palate (Midtgard 1984a). The right and left lateral branches off the medial palatine artery pass ventrally over the palatine branch of the palatomaxillary artery and anastomose into the lateral palatine plexus, which extends across the submucosa along the medial aspects of the maxillae and the medial aspects of the maxillary processes of the premaxillae, both of which form the tomial crests. 150 Toward the rostral aspect of the bony palate, the lateral ridges defining the median palatal groove each give off rostrolaterally oriented bony ridges. These ridges extend far rostrally, then strongly curve laterally, and then curve caudally and run caudally toward the rostral aspects of the lateral palatal grooves (before these grooves bend sharply lateral).

Branches of the medial palatine artery, accompanying veins, and palatal rami of the medial nasal nerves, course along the ventral aspects of these ridges. A series of ridges extend from the outer aspects of the above described, larger ridge, especially along the inside of the laterally oriented curve, and each of these ridges sharply curve caudally and occupy the bony spaces between the lateral and median palatal grooves; again, arterial, venous, and nervous branches travel along the ventral aspects of these ridges, and branch off to form an anastomotic plexus across the rostral bony palate (Midtgard 1984a). Rostral to the origin of the larger rostrolateral ridge, the lateral ridges defining the median palatal groove give off a series of smaller rostrolaterally oriented ridges, which become increasingly denser near the terminus of the median palatal groove, filling the bony area of the rostrolateralmost spaces of the bony palate, and each of which carries a neurovascular bundle on their ventral aspects.

These smaller neurovascular bundles course toward the dense tomial plexus and anastomose within them. Additionally, from each bundle, the small arteries send off and the veins receive a series of fine rostral and caudally directed vessels that anastomose with vessels from the parallel-running, laterally-oriented neurovascular bundle; the complex anastomoses create a fine, whispy, vascular plexus throughout the palatal submucosa between the tomial crests and the median palatal groove (Midtgard 1984a).

Upon passing rostral to the median palatal groove, the neurovascular bundle that ran through it, breaks up into a vast array of branches that pass to the rostralmost aspect of the 151 median component of the rostral bony palate. The very tip of the bony palate is occupied by

a dense array of grooves, rostrocaudally oriented in the median plane and rostrolaterally

oriented lateral to the median plane, all of which are occupied by fine neurovascular bundles.

A plethora of very fine foramina are found within these grooves, and provide access for the

neurovasculature to the external aspect of the bony tip of the rhamphotheca (which is

covered with small foramina). Caudal to this array of grooves, traversing lateral to medially,

the bony palate, is a series of foramina penetrated by various neurovascular bundles, and

which lead to the dorsum of the rostral aspect of the bony beak.

Palatine Nerve and Artery As discussed above, branches of the dorsal alveolar nerve and artery enter a small

foramen in the maxillary process of the palatine bone. Upon exiting this foramen, the

neurovascular bundle travels in a rostrolateral direction toward the rostroventral process of

the maxilla, passing through the submucosa of the caudolateral rhamphotheca, and finally,

ramifying into the caudalmost area of the lateral palatine plexus which is located in the

submucosa medial to the caudal rhamophothecal lamellae. The artery and its branches travel

dorsal to the nerve and its branches.

The ventral branch of the dorsal alveolar artery and nerve, the lateral palatine artery and the palatine nerve, respectively, pass through a large fissure located between the rostral aspect of the maxillary process of the palatine medially, the medial aspect of the jugal process of the palatine laterally, and the caudolateral aspect of the premaxillary process of

the maxilla rostrally. It is important to note, that although birds no longer have an

ectopterygoid, this fissure corresponds to the bony borders of the diapsid suborbital 152 fenestra, and as in other diapsids, the palatine neurovasculature passes through the rostral aspect of the suborbital fenestra.

Within the “suborbital” fissure, the lateral palatine nerve and artery both divide into two branches, first a large branch that passes through the fissure to the palatal surface, and the second, the main continuation of the artery (and nerve), being a larger, thicker branch

(the artery being much smaller than nerve). Upon exiting the fissure, the artery and nerve immediately fan out into a series of branches that stretch out toward the maxilla rostral to the bone’s caudoventral process (the artery and its branches positioned dorsal to the nerve and its branches). The arteries anastomose into the lateral palatine plexus, medial to the lamellae, rostral to the area supplied by the more caudal palatal branch of the dorsal alveolar artery.

Within the fissure, the continuations of the palatine artery and nerve enter and pass through a canal, which is primarily formed by a thin sheet of bone that passes from the medial aspect of the premaxillary process of the maxilla over the groove for the palatine nerve and ends at the lateral aspect of the premaxillary process of the maxilla. The nerve and artery continue to travel through a deep and wide groove in a sharp rostrolateral direction. The groove is situated between the rostromedial aspect of the premaxillary process of the maxilla and the caudomedial palatal process of the premaxilla. Through their course, the artery and nerve give off a dense array of lateral and then caudolateral branches, with the nerve branches innervating most of the lamellae and the artery supplying the lateral palatal plexus rostral to the areas supplied by the two more caudal large palatal arteries.

Medial branches off the palatal artery anastomose into the fine plexus extending across the rostral bony palate. The lateral palatal groove, and the neurovasculature that formed it, end 153 at the rostrolateralmost aspect of the maxillary bone, where some specimens possess a kink between the maxilla and premaxilla. The final and lateralmost branches of the lateral palatine neurovascular bundle pass laterodorsally through the notch, or over the tomial crest, and ramify across the laterodorsal areas of the maxilla and premaxilla forming the rostral beak.

The more rostromedial branches of the lateral palatine nerve and artery are very long structures, with a more directly rostral orientation, that continue along the submucosa of the rhamphotheca ventral or medial to the lamella, and provide branches that innervate and supply the most rostral lamellae and lateral palatine plexus, eventually reaching the rostrolateralmost bony palate and giving some branches to the dorsal aspect of the rostral rhamphotheca through small foramina. The larger of these vessels leave rostral and rostrolaterally oriented grooves along the ventrolateral premaxilla.

Nasal Cavity The olfactory nerve and ethmoidal vessels pass into the orbit from the rostral cranial fossa through the olfactory foramen, the vessels being just lateral to the nerve. The neurovascular bundle courses rostrally across the dorsomedial aspect of the orbit through a deep groove in the dorsal osseous interorbital septum, the olfactory sulcus. More rostrally, the olfactory sulcus in ducks is subdivided into a shallow dorsal channel and a much deeper ventral channel. The olfactory nerve travels through the ventral channel, and is enclosed by a thick tissue derived from the interorbital septum that is variably ossified. The vessels occupy the entire lateral aspect of the olfactory sulcus, from the dorsal margin of the shallow dorsal groove, to the ventrolateral aspect of the olfactory nerve. The ethmoidal vessels anastomose with the supraorbital vessels (as well as the cerebral ethmoidal artery) shortly upon exiting the external olfactory foramen to form the nasal artery and vein (Assenmacher 154 1953; Richards 1967; Baumel 1975, 1993; Midtgard 1984a). The ethmoidal artery is smaller

than, and originally lateral to the ethmoidal vein, and then travels ventral to and around the

vein to lie in a position lateral to it.

The olfactory nerve, accompanied by small vessels, travels rostrally into a laterally

open fossa within the dorsal aspect of the main body of the mesethmoid, situated rostral to

the mesethmoidal ridge and caudoventral to a lateral process of the dorsal lamina of the mesethmoid. The medial aspect of the caudal nasal concha projects into this lateral mesethmoidal fossa, lateral to the olfactory nerve and vessels. Branches of the olfactory nerve and vessels travel lateral and dorsally across the caudal concha and onto the tectum nasi cartilage (Watanabe and Yasuda 1968).

At the rostral aspect of the orbit, after passing to the rostral aspect of the orbit, the

profundus nerve arches over the dorsomedial ectethmoid, rostrolateral to the olfactory nerve

aperture, and divides into lateral and medial nasal nerves (Witmer 1995b). Figure 6A and B

depict the course of the medial and lateral nasal arteries in the nasal cavities. The medial

nasal neurovascular bundle immediately enters the medial orbitonasal foramen in the

ectethmoid (Witmer 1995b). The ectethmoid and the medial orbitonasal canal are situated

dorsal and lateral to the tectum nasi, and as such, the medial nasal neurovascular bundle is

osseously separated from the olfactory nerve within the lateral mesethmoidal fossa in its

rostral course. In anseriforms, the lamina dorsalis of the mesethmoid develops into a lateral

process that curves ventrally to form a short wall of bone paralleling the main body of the

mesethmoid. This lateral mesethmoidal wall separates the medial and lateral neurovascular

bundles from each other, and forms the lateral wall of the medial nasal canal, and the medial

wall of the lateral nasal canal. The ventral aspect of the lateral mesethmoidal wall curves 155 medially and then dorsally to form the ventral and medial osseous walls of the medial nasal canal, and the frontal forms the canal’s roof. The medial nasal vein travels medial to the nerve, and the artery is originally lateral to it. The medial nasal canal ends rostral to the lateral mesethmoidal fossa, and upon exiting the rostral medial nasal foramen, the medial nasal neurovasculature becomes compressed against the nasal mucosal lining of the lateral aspect of the mesethmoid, in a position medial to the caudal concha, toward and into which the bundle gives off laterodorsally oriented nerves and vessels.

Anatomy and Vasculature of the Nasal Vestibule Rostral to the caudal concha, the neurovascular bundles give branches to the middle nasal concha. The vessels associated with the middle nasal concha form an extremely dense plexus within the conchal submucosa. The rostralmost aspect of the dorsal lamina of the mesethmoid serves as an area of articulation with the tectum nasi (the cartilaginous roof of the nasal cartilages), and ventral (and in some areas caudal) to this area, the bony nasal septum articulates with the caudal aspect of the cartilaginous nasal septum. The tectum nasi spreads out laterally from the nasal septum, across the ventral aspect of the nasal bone. Far laterally, the tectum nasi curves ventrally with the nasal bone and then across the premaxillary process of the maxilla ventral to its articulation with the nasal bone. In its ventral curvature, the tectum nasi covers the dorsolateral wall of the nasal vestibule, caudal to the bony internal nares. Protruding laterally into the dorsal nasal vestibule from this lateral wall, formed by the tectum nasi, is the rostral concha.

The dorsal and ventral aspects of the tectum nasi further present a complicated anatomy. A long groove runs longitudinally across the middle of the dorsal tectum nasi.

Through the cartilage, large vessels were seen that run ventral to the cartilaginous groove. 156 Ventral to the cartilaginous groove is a longitudinally running, central fold between the nasal

septum and the tectum nasi. Again, on the ventral aspect of the tectum nasi, lateral to the

central fold, is a second longitudinally running ridge. This lateral ridge is actually the thin, rostral extension of the middle concha. The rostral aspect of the middle concha, before tapering into a ridge, is a densely vascular bulbous structure. The dorsal aspect of the tectum nasi, above the lateral ridge, is characterized by a long, longitudinally running lateral groove.

Through the cartilage, another large vessel(s) can be seen to run ventral to the groove and within the ventrolateral ridge.

In Anas, the nasal crest originates along the caudodorsomedial (nasal) aspect of the

premaxillary process of the maxilla, just caudal to the narial opening of the palatine fenestra.

The bone expands rostrodorsally and caudodorsally from a caudoventrally directed point,

and then expands from the rostrodorsal aspect, appearing as a long triangular object with the

point facing rostrally. This rostral point is suspended over the caudal aspect of the palatine

fenestra. Between the area dorsal to the premaxillary process of the maxilla and ventral to

the rostral end of the nasal crest is a wide unossified space, which is filled by a thin

cartilaginous sheet The cartilage of the tectum nasi passes over the dorsal aspect of the nasal

crest.

Rostral to the middle concha and caudal to the rostral concha is a large, thick,

transversely oriented ridge that originates from the dorsolateral aspect of the premaxillary

process of the maxilla, at the caudal aspect of the bony internal nares, and runs medially

toward the nasal crest. Since this ridge runs across the floor of the nasal cavity, it is covered

with mucosa that is continuous with the solum nasi. The ridge effectively divides the nasal

cavity into two anatomical areas, with the rostral slope of the ridge forming the caudal aspect 157 of the nasal vestibule and the caudal slope forming the rostral aspect of the nasal choanal

recess. A small, dorsomedially inflected crest on the dorsomedialmost aspect of the

transverse nasal ridge projects toward, but does not reach, the nasal crest. There is a large

gap between the horizontal ridge and the nasal crest. On the lateral aspect of the nasal crest,

near its dorsal end, is a longitudinally running ridge that project laterally into the caudal nasal vestibule. The mucosa of the nasal septum, which covers the lateral ridge along the nasal crest, runs ventrolaterally and becomes continuous with the mucosa of the transverse nasal crest. A large, thick, dorsally oriented mucosal pillar is formed by the mucosal bridge connecting the longitudinal ridge of the nasal crest and the horizontal ridge of the maxilla.

These three connected ridges greatly increase the mucosal surface area of the nasal vestibule;

however, the series of mucosal folds are actually more elaborate. The mucosa along the

lateralmost aspect of the horizontal nasal ridge continues as a fold that runs rostrodorsally

toward the rostral concha, and then continues to run rostrally as a ventral, medially

projecting ridge off the rostral concha. The dorsalmost aspect of the mucosal pillar is partly

formed by the bulbous medial component of the middle concha.

A second, more rostral, horizontal ridge, on the narial aspect of the premaxillary

process of the maxilla, runs medially across the nasal vestibule toward the nasal crest. This

second crest is caudal and lateral to the premaxillary fenestra. As with the caudal horizontal

ridge, there is a gap between the ridge and the nasal crest. A sheet of mucosa associated

with the longitudinal ridge of the nasal crest runs rostroventrally to become continuous with

the rostral horizontal ridge, forming a rostral horizontal pillar.

In lateral view, the rostral nasal septum forms a semicircular structure, that curves

caudodorsally from the caudal border of the premaxillary fenestra, and then curves 158 rostrodorsally to meet the tectum nasi in an area in line with the rostral aspect of the bony

internal nares. As a result, the dorsal component of the rostral nasal septum is rostrally

much longer than the caudal component. The nasal crest forms part of the rostral septum.

The mucosa of the rostroventral tectum nasi spreads along the sides and ventral aspect of

the rostrodorsal septum, and is then continuous with a sheet that runs ventrally across the

rostral border of the septal semicircle, and is finally continuous with the solum nasi covering

the floor of the nasal vestibule (as well as covering over the premaxillary fenestra).

As it nears the mesethmoid’s area of articulation with the tectum nasi, the medial

nasal artery gives off branches dorsal to the medial nasal nerve and forms vessels that then

pass on the medial aspect of the nerve. At the caudalmost aspect of the tectum nasi, the neurovascular bundle curves ventrally away from the tectum along the mucosa. Past the mesethmoid, the medial nasal nerve becomes compressed against the cartilaginous nasal septum, and the medial nasal artery gives off branches into, and the vein receives vessels from, a dense vascular plexus spread across the septal mucosal. On the mucosa dorsal to the middle concha, the medial nasal artery gives off a series of lateral branches to the middle

concha which ramify into a massive vascular plexus, which in turn sends off dorsal branches

into an extremely dense vascular plexus associated with the mucosa of the crista nasalis and

which anastomoses into and feeds the vascular plexus associated with the rostral concha.

The mucosa rostral to the pharyngeal infundibulum is continuous with the mucosa

lining of the vomer and caudal nasal cavity. Through the submucosa, vessels from the

sphenopalatine artery pass across the premaxillary process of the maxilla, ventral to the nasal

septum, and travel rostrally. These arteries supply the ventral aspect of the caudal concha,

and send off rostral branches that pass to the ventral aspect of the middle concha. As the 159 medial nasal artery approaches the nasal crest, it anastomoses with branches of the sphenopalatine artery. The resulting artery immediately sends off branches that ramify through the submucosa on the lateral aspect of the nasal crest, and more ventrally, the submucosa of the solum nasi.

In its course across the nasal septum, the medial nasal nerve and its associated vasculature curve rostroventrally from their dorsal position toward the floor of the nasal cavity (Midtgard 1984a). Upon reaching the nasal cavity floor, the nerve runs rostrally through the submucosa of the solum nasi, and early in its course, travels medial to the caudal mucosal pillar. The nerve then continues its rostral course, traveling along the cartilage that spans the area between the dorsal maxilla and the nasal crest.

Along the medial nasal nerve’s descent along the nasal septum and, caudolateral to the nasal crest, the medial nasal artery gives off two major branches that ramify within the plexus associated with the dorsal area of the caudal pillar and the rostromedial middle concha. The ventral branch courses along the medial aspect of the medial nasal nerve, and supplies the ventral nasal septum, the ventral areas of the caudal and rostral mucosal pillars, and gives off branches into the dense vasculature within the submucosa of the solum nasi.

The more dorsal branch of the medial nasal artery, the septal artery, divides into medial and lateral septal branches. Both branches give off numerous branches that anastomose within the nasal septum submucosa. The lateral septal branch, which is more dorsal, travels rostrally, dorsolateral to the nasal septum, and is closely paired with the lateral septal branch from the opposite side. The two lateral septal branches run ventral to the median longitudinal groove of the tectum nasi. The medial septal artery runs rostroventrally to meet the medial septal artery of the opposite side, and the two vessels course rostrally, within the 160 submucosa that is ventral to the long rostrodorsal process of the nasal septum. The venous

drainage of the septal areas follows along the arteries.

A more caudal branch of the medial nasal artery, that supplies and runs along the

dorsomedial aspect of the middle concha, and is related to the middle conchal cavernous

tissue, travels dorsal to the medial nasal artery toward the caudal nasal crest. In its course,

the vessel travels medial to the rostromedial bulb of the middle concha, and bifurcates in the

rostralmost area of the bulb. The more lateral branch, the rostral conchal artery, travels

rostrolaterally to form the main blood supply to the cavernous tissue associated with the

rostral concha. This branch primarily travels along the lateral wall formed by the

ventrolateral tectum nasi. The more medial branch, the ventral tectal artery, runs dorsal to

the fold that acts as a rostral extension of the middle concha, and passes along the ventral

tectum nasi. It is likely that the rostral extension of the middle concha is actually formed by

the artery that passes dorsal to it. In its course, the lateral tectal artery sends off lateral

branches that anastomose with branches of the rostral conchal artery, and sends off medial

branches to a plexus ventral to the tectum nasi and fed by the lateral septal artery.

The medial nasal nerve, artery, and vein pass through the submucosa medial to the

rostral horizontal pillar between the rostral horizontal ridge and the rostroventral nasal crest.

The neurovasculature then continues rostrally into the submucosa that is spread across the

premaxillary fenestra, so the nerve passes rostrally between the floor of the nasal vestibule and the roof of the oral cavity. Shortly after passing the caudodorsal border of the premaxillary fenestra, the nerve, artery, and vein divide into lateral and medial branches. The medial branch of the medial nasal nerve travels rostroventrally into the oral cavity and was described above, whereas the larger lateral branch passes rostrally through the submucosa of 161 the narial face of the premaxillary fenestra toward the rostral aspect of the nasal vestibule.

The oral component of the medial nasal artery anastomoses with the median palatine artery, and the oral vein off the medial nasal vein anastomoses with the medial palatine vein

(Midtgard 1984a). In its rostral course, the medial nasal vessels supply and drain the rostral solum nasi. Finally, the neurovascular bundle enters a foramen in the ventrolateral aspect of the premaxilla in the area where the bone forms the rostral border of the nasal vestibule.

Before exiting the nasal vestibule, the arteries and veins send off branches that anastomose with branches of the lateral nasal vasculature as the lateral nasal neurovasculature exits the nasal vestibule. The medial nasal neurovasculature courses through a canal in the rhamphothecal component of the premaxilla (Midtgard 1984a), sending off a series of smaller, nutrient neurovascular bundles to the outer rhamphotheca. Toward the end of the premaxilla, the small vascular remnants of the medial nasal neurovasculature ultimately anastomose with remnants of the lateral nasal vasculature, and with dorsal rhamphothecal branches of the median palatine artery (Midtgard 1984a). This resulting plexus of vessels escapes from the internal premaxilla through nutrient foramina in the rostralmost rhamphotheca and supplies and drains this sensitive area.

The lateral nasal neurovascular bundle passes over the lateral process of the ectethmoid, and against the medial and dorsal aspects of the lacrimal bone. The neurovascular bundle then travels rostrally through a ventrally incomplete osseous canal

(Witmer 1995b), the lateral orbitonasal canal, medial to the medial aspect of the lacrimal, against the lateral face of the short lateral mesethmoidal wall, and against the ventral aspect of the frontal; a ventral and laterally inclined ridge encloses the bundle medially. A thick, apparently cartilaginous, tissue lining forms a floor to the lateral nasal canal. Near the rostral 162 end of the mesethmoid, the neurovascular bundle exits the lateral nasal canal, and the bundle travels rostrally across the dorsal aspect of the tectum nasi mucosa, and ventral to the nasal gland ducts and the perisosteum of the nasal bone (Witmer 1995b). In their course, the lateral nasal artery gives off medial branches to, and the vein receives vessels from, a groove running across the dorsal midline of the tectum nasi. Further rostral, the vessels supply and drain the plexus of the rostral concha (Midtgard 1984a). The neurovascular bundle then enters into a dorsomedial foramen within the premaxilla, situated in and facing into the rostralmost area in the nasal vestibule.

Brief Overview of the Cephalic Venous System Most of the arteries described above are accompanied in their pathways by veins that drain along the arteries, and for this reason most of these venous structures were not explicitly described. Some of these vessels were discussed in relative detail, especially in cases where their course deviated from the arterial pattern. However, because the above description focuses on arteries and their pathways of supply, we present the following sketch of the drainage pattern of the major cephalic veins, following a rostral to caudal order of description. Since many of these vessels were previously discussed in relation to the arterial system, they will not be described at the level of fine detail as were the arteries.

Just medial to the rostromedial aspect of the lamellae, the lateral palatine vein courses caudomedially toward the bifurcation of the submandibular artery into lateral and medial palatine arteries. Along the medial aspect of the rictus, the lateral palatine vein receives the rictal vein, which in turn drains the dorsal and ventral rictal veins (Midtgard

1984a). The ventral rictal vein drains from the lateral aspect of the mandible and creates a deep groove in its course. At the caudolateralmost aspect of the pterygoid process of the 163 palatal process of the maxilla, the medial palatine vein curves caudolaterally to course across the ventral aspect of the maxillary process of the palatine, toward the bifurcation of the submandibular artery, and then courses caudomedially across the dorsal aspect of the artery.

Caudal to the bifurcation of the submandibular artery, the medial and lateral palatine veins

anastomose and the resulting palatine vein courses along the submandibular artery to the

caudal aspect of the lateral palatine fossa of the palatine bone. In this region, the rictal vein

anastomoses with the palatine vein which forms the maxillary vein (Baumel 1975, 1993;

Midtgard 1984a). Just caudal to this, the maxillary vein receives the dorsal alveolar vein, and

then, further caudal, receives the orbitonasal vein which drains the antorbital sinus and

portions of the nasal cavity. In its course toward the maxillary vein, the orbitonasal vein

travels ventrally across the caudodorsal aspect of the palatine fossa.

The maxillary vein then continues to course caudoventrally across the rostrodorsal

aspect of the pterygoid and receives the ophthalmic vein which drains much of the orbit and

the nasal cavity (Baumel 1975, 1993; Midtgard 1993). As the maxillary vein drains caudally

across the dorsomedial aspect of m. pterygoideus ventralis, the vessel receives the

temporomandibular vein (Richards 1967; Baumel 1975, 1993; Midtgard 1993), forming the

rostral cephalic vein.

The jugal vein courses caudally across the medial aspect of the jugal, and then

caudomedially toward the rostrolateral aspect of the quadratoarticular joint, and in this area

receives the mandibular vein to form the maxillomandibular vein. The maxillomandibular

vein passes medially across the quadratoarticular joint, receives the rostral auricular vein,

forming the temporomandibular vein medial to the joint capsule, and then courses

caudomedially around the medial aspect of the articular bone. 164 The rostral auricular vein courses caudoventrally across the caudolateral ridge of the mandibular process of the quadrate, then passes medially across the caudolateral extension of m. protractor quadratus along the caudal aspect of the quadrate mandibular process in a position dorsal to the mandibular condyle, and then travels rostrally across the medial aspect of the mandibular process. At the rostromedial aspect of the process, the rostral auricular vein drains into the maxillomandibular vein. The maxillomandibular vein further receives a vein draining ventrally from the ophthalmic rete in this region.

Upon receiving the temporomandibular vein, the rostral cephalic vein courses caudomedially across the ventrolateral basisphenoid toward the lateral aspect of the basiparasphenoid and the rostrolateral aspect of m. rectus capitis ventralis pars medialis.

Upon reaching the muscle, the vein receives a caudally directed vessel that drains the sphenopalatine and sphenomaxillary veins. The vessel draining the sphenopalatine and sphenomaxillary veins courses to the basicranial region from the lateral aspect of the parabasisphenoid. See Table 1 for the terminology used for the craniocervical musculature in this dissertation, and a list of commonly used synonyms.

The rostral cephalic vein courses caudally along the ventral aspect of m. rectus capitis ventralis pars medialis and across the ventrolateral aspect of the esophagus. The left rostral cephalic vein then sends off a large vein that courses caudomedially across the ventral aspect of the left m. rectus capitis ventralis pars medialis to the mid-ventral aspect of the right muscle belly and drains into the right rostral cephalic vein through the interjugular anastomosis (Richards 1967; Baumel 1975, 1993; Midtgard 1993). At this point, the lateral right aspect of the interjugular anastomosis receives the internal carotid vein which travels ventrally from the external ostium of the cranial carotid canal and along the internal carotid 165 artery. The resulting right jugular vein then continues to course caudally across m. rectus capitis ventralis pars medialis and eventually receives the common occipital vein. The left rostral cephalic vein is continued by the much smaller left jugular vein (Richards 1967;

Baumel 1975, 1993; Midtgard 1993).

The lingual vein drains dorsally into rostral cephalic vein sinistra just caudolateral to the latter vessel’s drainage into the right rostral cephalic vein (Baumel 1975, 1993; Midtgard

1993). The right lingual vein drains into the jugular vein just caudal to the interjugular anastomosis (Baumel 1975, 1993; Midtgard 1993).

The bony endocranial margins of the foramen magnum are encircled by a single large venous sinus formed by the anastomotic relationships between the occipital sinus, the basilar sinus and the system of vertebral sinuses. A large vein branches from the ventrolateral aspect of the occipital sinus and bifurcates into a ventral and a lateral vein. The lateral vein courses laterally across the caudal aspect of the exoccipital and anastomoses with the external occipital vein to form the common occipital vein which immediately sends off a caudal branch that drains caudally through the craniocervical musculature and which receives a ventrally inclined vessel that receives several branches draining the dorsal craniocervical musculature.

The ventral continuation of the common occipital vein drains ventrally across the caudolateral aspect of the exoccipital, the caudomedial aspect of the squamosal, and lateral to the hypoglossal foramina, and receives veins that drain from these foramina and travel along the hypoglossal nerves. In this course, the vein travels across the rostral aspect of a common aponeurosis for mm. complexus and splenius capitis. 166 After draining through the external occipital foramen, the external occipital vein courses ventrolaterally across the caudomedial aspect of the supraoccipital, across the rostral aspect of the common aponeurosis for mm. complexus and splenius capitis, then travels across the caudomedial aspect of the exoccipital and finally anastomoses with the lateral branch of the foramen magnum sinus.

As the left common occipital vein courses across the parabasal fossa, the vein receives the caudoventrally inclined left stapedial vein and the left internal carotid vein, and forms the caudal cephalic vein (Baumel 1975, 1993). Similarly, the right common occipital vein receives the right stapedial vein in this region, but not the internal carotid vein. The caudal cephalic vein drains caudoventrally and directly into the common jugular vein

(Richards 1967; Baumel 1975, 1993; Midtgard 1993) .

The ventral branch of the foramen magnum sinus, the ventral occipital vein, courses ventrally across the lateral aspect of the occipital condyle across the medial aspect of m. rectus capitis dorsalis, and then courses ventromedially across the ventral aspect of the occipital condyle and the dorsal aspect of m. rectus capitis ventralis pars lateralis. Further rostromedial, the vein travels across the dorsal aspect of m. rectus capitis ventralis pars medialis and anastomoses with the contralateral ventral occipital vein.

In the basicranial region, a series of veins drains ventrally from a vein that courses through the notocordal crest and passes via a dense array of foramina in the ventral aspect of the basioccipital into a deep fossa in the caudoventral basioccipital. This fossa is located rostrodorsal to the rostroventral aspect of the occipital condyle, caudodorsal to the caudoventral aspect of the parabasisphenoid, and dorsomedial to the basioccipital basal tubera. Within the rostral aspect of the fossa, the “notocordal” veins drain into a large 167 median vein, the basicranial vein, formed by the anastomosis of the left and right ventral

occipital veins. The basicranial vein further receives a plexus of veins that expands across

the ventral aspect of the basiparasphenoid and the dorsal aspect of m. rectus capitis ventralis

pars medialis. Subsequent to receiving the veins in the basicranial area, the basicranial vein

drains ventrally between the medial aspects of the two muscle bellies of m. rectus capitis

ventralis pars medialis to the ventromedial aspect of these muscles and drains into the dorsal

aspect of the left vein rostrolateral to the latter vessel’s drainage into the interjugular

anastomosis.

Discussion

The Apomorphic Avian Head

Unique Traits in Bird Skulls The head skeleton of extant birds is readily distinguishable from other sauropsids by

significant bone loss, reduction, and fusion, an enlarged orbital fossa, an inflated endocranial

cavity, and an elongated rostrum (Zusi 1993). Extant birds lack a postorbital bone, the

postorbital process of the jugal, and the squamosal process of the quadratojugal, which

creates an open communication between the orbit and the former lateral temporal and dorsal temporal fossae (thus, losing the typical diapsid architecture). The avian pterygoid

and maxilla have become greatly reduced in comparison to other sauropsids. Additionally,

birds differ from other sauropsids, including their extant sister taxon, Crocodylia, in the

absence of prefrontal, ectopterygoid, and coronoid bones.

It is important to remember that the head skeleton is molded by and acts as a

scaffold to support and to protect the various soft tissues of the head; thus, significant

changes in the head skeleton reflect significant changes in other cephalic tissues and tissue 168 systems. Two soft-tissue structures in birds, the eye and brain, have become greatly

modified from the ancestral sauropsid or archosaurian condition. In comparison to other

sauropsids, birds have greatly enlarged brains. De Beer (1937) noted that the shape of the

braincase is dependent on the volume of its contents. Nicholas (1930, cited in De Beer)

demonstrated that the increased pressure created by replacing the midbrain by grafting in

rapid growing tissue such as pronephros rudiments causes the early cranial cartilages to expand to make room for the growing pronephros. In mammals, atrophy of the brain is known to result in overdevelopment of the nasal sinuses and cranial vault thickening (Ross

1941). In a study of human hemipelagic patients, Ross (1941) found that regions overlying atrophic components of the brain resulted in diminution of cranial volume, overpneumatization of the supraorbital, mastoid, and petrous air cells, and either extreme

thickening or thinning of the portion of the cranial vault overlying the atrophic tissue. A

similar study by Dyke et al. (1933) found that such brain atrophy further resulted in

enlargement of the ethmoid, mastoid, and frontal sinuses. Based on the results of

experimental research performed on rats, Young (1959) hypothesized that an expansion of

the cranial contents creates intracranial pressures which translate into tensile forces in the

surrounding tissues, which can lead to modifications in the shape, size, and spatial

arrangements of functionally related tissues such as dura, muscle, and bone.

In extant birds, as the cerebrum increases in size, the individual bones of the

endocranium change to accommodate it. For instance, with the enlargement of the cerebral

frontal and parietal lobes, the parietal and frontal bones become much larger and greatly

deepen and expand the rostral cranial fossa. Also, as the cerebrum increases in size, it pushes

the mesencephalon ventrally and the cerebellum caudoventrally. With the anatomical 169 displacement and re-orientation of the hindbrain, the cranial bones associated with these

areas similarly change and attain a morphology and orientation that appears very different

from the ancestral positions exemplified by crocodilians. Though there are some aspects of

avian brain enlargement that are complicated, such as the ventral displacement of the

mesencephalon, this anatomical transformation is, in many ways, only superficially complex.

In birds, the endolymphatic duct appears to be just rostral to the ventralmost aspect of the

rostral semicircular eminence, whereas in crocodilians the duct is just ventral to the ventral

aspect of the eminence. Again, in birds the external occipital foramen is caudodorsal to the

rostral semicircular eminence, whereas in crocodilians the external occipital foramina are

rostrodorsal to the eminence. Obviously, both of these examples demonstrate endocranial

rotation in birds.

The caudoventral movement of the cerebellum results in a clockwise twisting of the

caudal, and part of the rostral, encephalic skeleton. When the medial aspect of the right side

of a sagittally sectioned modern bird skull is turned counterclockwise, the endocranial

skeleton is remarkably similar to the ancestral archosaurian condition, and differs little from

the crocodilian braincase.

The laterosphenoid is an excellent example of this: the bone is related to the

cerebrum and the mesencephalon. The rostral aspect of the laterosphenoid forms a large

component of the rostral cranial fossa in birds, and most of the fossa in crocodilians and

many other non-avian archosaurs (e.g., Proterosuchus, Erythrosuchus, Euparkeria, most basal avesuchians, and even theropods phylogenetically close to birds such as Allosaurus ). The movement of the mesencephalon and expansion of the cerebrum shift the laterosphenoid rostrally and ventrally. The tentorial crest runs across the vertical axis of the ancestral 170 archosaurian laterosphenoid, and the sphenotemporal sinus travels across it. The ventral

aspect of the tentorial crest cleaves between the caudoventral surface of the cerebrum and

forms the rostral border of the maxillomandibular fossa. Further dorsal, the protuberantia

tentorialis cleaves between the caudodorsal cerebrum and the rostral surface of the optic

tectum. In birds, the crest has become horizontally oriented and, proximal to developing into the protuberantia tentorialis, the crest cleaves between the ventral surface of the cerebrum and the dorsal surface of the optic tectum. In birds, the internal maxillomandibular fossa rests within the caudolateral aspect of the middle cranial ( = mesencephalic) fossa. As the avian cerebrum has turned caudoventrally from the ancestral position, the ventral surface of the avian cerebrum is the caudal surface of non-avian archosaurs. Thus, the avian positionally altered tentorial sinus, which is oriented almost perpendicular to its position in crocodilians, drains and rests against the same tissues as the crocodilian sinus.

Avian brain evolution has, of course, resulted in osteological transformations that

greatly deviate from the ancestral archosaur braincase, and these transformations correlate

with biologically important changes in vascular supply and drainage of the brain. For

instance, in crocodilians, the protuberantia tentorialis and its associated dura cleave between

the caudodorsolateral surface of the cerebrum and the rostrodorsolateral surface of the optic

lobe. This was likely the anatomy in other non-avian archosaurs, including non-avian

theropods (e.g., Allosaurus), based on the position of the mesencephalic fossa. In birds,

however, the protuberantia tentorialis and marginal crest cleave between the cerebrum and

the rostrodorsolateral surface of the cerebellum, and, as a result, the transverse sinus and the

large torcular heropholi drain and rest across the cerebellum rather than the optic lobes. If 171 whole brain cooling via the dural sinuses is a possibility in archosaurs, then the transverse sinus and torcular heropholi of birds and non-avian dinosaurs are involved in the temperature regulation of very different neural regions, with potentially quite different biological implications.

Both the example of the tentorial and the marginal crests emphasize that the identification of various important encephalic vessels in fossil specimens is dependent on the preservation of endocranial crests and ridges. Since many of these crests are formed by the ossification of dura, the interpretation of these structures is complicated by the differential ossification of the dura between ontogenetic stages, individuals, and clades. This can be especially difficult when studying many basal fossil archosauromorphs, many of which ossify the endocranium very little (e.g., rhynchosaurs). The tentorial crest of hatchling and juvenile ducks, geese, and ostrich is frequently unossified or poorly developed. Occasionally, as seen with the course of the rostral petrosal sinus, the ossified dura will form a bony canal for the vessel, and the amount of ossification can be quite variable between adults within a population. However, many of the dural crests have osteological relationships that are consistent between clades. For example, the marginal crest always runs horizontally across the caudoventral surface of the parietal, and the protuberantia tentorialis runs across the caudolateral aspect of the parietal. Thus, an understanding of the osteological correlates of non-vascular structures, such as dural sheets, or even an understanding of the bony relationships of infrequent vascular osteological correlates, such as the tentorial crest, and their anatomical transformations over ontogeny and phylogeny can allow for their reconstruction and the reconstruction of the associated vessels in fossils. 172 This also applies to non-dural vessels the caudoventral cerebellar artery supplies the

cerebellar auricle, part of the medulla, gives off the labyrinthine arteries, and supplies a large

expanse of the cerebellum. In all crocodilians and birds studied, the caudoventral cerebellar

artery courses laterally across the caudodorsal surface of the basisphenoid just rostral to the

basisphenoid-basioccipital suture.

In both birds and crocodilians, the rostral division of the accessory nerve and the

endolymphatic sac limit the size and define the shape of the occipital sinus. Both of these

soft-tissue structures have clear osteological correlates which are described in the section on

encephalic vasculature.

Occasionally, remarkable ossification in a fossil will greatly enhance our ability to

trace character states. In the pterosaur Tapejara, the falx cerebri has actually ossified into a frontal crest, and the two well developed marginal crests join the former crest, forming a slight Y-shape. Each marginal crest ventrally becomes the protuberantia tentorialis. The appearance of this system of crests, and likely the sinuses associated with them, is nearly identical to the anatomy of Anas, a species in which these dura are typically well ossified.

This study found a remarkable number of similar encephalic vessels with clear

osteological correlates between extant crocodilians and birds, providing a level one inference

for the particular vessels, including all of the dural venous sinuses listed in the Nomina

Anatomica Avium. Additionally, many of these osteological correlates could be further

identified in several fossil archosaurs, and passed the congruence test of homology. Many of

the correlates were ubiquitous in fossil archosauromorphs (e.g., rostral petrosal sulcus,

external occipital vein foramen, auricular foramen), and were clearly present in basal forms 173 such as Mesosuchus, a basal rhychosaur. These vessels and their osteological correlates are

listed in Table 3.

Orbit Extant birds have extremely large eyes. De Beer (1937) reviewed several studies that

demonstrate the significant role the eye has in shaping the size and shape of the skeletal

orbit. Hanken (1983) showed in the miniaturized Thorius that the rostral braincase walls are deflected inwardly to conform to the margin of the eyes. Hanken showed that the eyes of

Thorius limit the lateral expansion of the rostral aspect of the brain itself. Additionally, the close contact of the eyes in Thorius displaces the nasal capsules forward. Coulombre and

Crelin (1958) demonstrated that the growth of the eye greatly influences the shape, size, and position of the orbital bones and exerted a mechanical influence beyond the orbit. Witmer

(1995b) found that the enlarged eye encroaches on the antorbital cavity and subsequently displaces the orbital process of the lacrimal bone rostrally and can further impinge upon the caudal portion of the nasal capsule (“telescoping” it) which can lead to loss of the caudal concha in some small bird species.

The rotation of the brain also rotates the external aspect of the laterosphenoid. The

laterosphenoid has shifted rostroventrally from its ancestral orientation. As a result, the

cotylar crest, the insertion of m. tensor periorbitae, and the proximal course of the

ophthalmotemporal vessels are horizontally rather than vertically oriented. Despite these

changes, however, the orbital blood supply in crocodilians and birds is remarkably similar,

including the course of the ophthalmotemporal artery through the ocular muscles and its

development of the periocular plexus. 174 Modification of Facial Anatomy In the course of avian evolution, the facial anatomy of birds has become greatly altered from the basal archosaurian condition. The changes in the nasal and palatal regions has had an influence on the nasal vestibular vascular plexus and the palatal blood supply.

Extant birds are further characterized by the development of an elongated edentulous rhamphotheca (though a rhamphotheca does not necessitate the absence of teeth). The bony skeleton supporting the rhamphotheca has become greatly modified. The premaxilla has developed a long prenarial component and the maxilla has become greatly reduced. The reduction of the maxilla appears to result from two major character changes:

(1) the loss of the dorsal ramus of the nasal process of the maxilla; and (2) the loss of teeth

(Witmer 1995b).

Vascular Physiological Devices and Brain Temperature Regulation There are a variety of possible effects of overheating the brain—including damage and even death. Anything that minimizes this should be of great value. In fact it is has been shown by Bech and Mitdgard (1981) that the Australian zebra finch, which has an underdeveloped ophthalmic rete, will die off in the millions during periods of high temperature. All the vascular structures discussed below appear, at least anatomically, to be well suited to act as thermoregulatory systems, specifically in reference to brain cooling.

There are two very different mechanisms of selective brain temperature regulation in amniotes—selective hypothalamic vs. whole brain cooling. Much of the past research has focused on selective hypothalamic cooling. In most cases, cool venous blood draining moist mucosal regions enters into a rete and through a countercurrent exchange of heat, cools blood that ultimately supplies the hypothalamus—the neural region responsible for temperature regulation. 175 This study recognized four large complexes of vascular physiological devices shared

by Crocodylia and Aves, most of which are comprised of smaller, interconnected, vascular

devices: (1) A series of orbital plexuses, including the ophthalmic rete; (2) the nasal

vestibular vascular plexus; (3) the erectile tissue of the middle ear; and (4) the buccopharyngeal plexus.

This section will discuss the evidence for brain cooling in birds, and will follow with

a discussion on the ophthalmic rete, a brief overview of non-orbital vascular devices, then

the suborbital diverticulum, and finally the nasal vestibular vascular plexus. Chapter 3 will discuss the buccopharyngeal vascular devices and provide a brief discussion on behaviors associated with these devices, namely gular flutter and mouth gaping.

Evidence for Brain Cooling

Richards (1970) studied the effects of heats stress on Gallus and recorded

temperatures in the hypothalamus and neostriatal region. Under normothermic conditions

both temperatures were lower than core body temperature, between a range of 0.6-1.1ºC.

Neostriatal temperature was lower than hypothalamic temperature by 0.2ºC. However,

during heat stress, the temperature difference between the brain temperatures decreased and

were similar to core temperature. When temperature was lowered to normal (15-22ºC),

hypothalamic temperature rapidly decreased. The decrease between core and brain

temperature occurred at the onset of panting and it would appear that the vascular

physiological devices responsible for brain cooling were switched off at this point. Richards

(1970) hypothesized that hypothalamic temperature was lower than core under

normothermic conditions because of countercurrent heat exchange between the intercarotid

anastomosis and the cavernous sinus. Richards pointed out that the intercarotid 176 anastomosis of Gallus was essentially within the cavernous sinus. The cooling of the intercarotid anastomosis would then cool the blood directly supplying the hypothalamus.

Richards felt that the most likely region of countercurrent cooling occurred in the ophthalmic rete and noted the extensive connections between the vessels of the rete and the brain.

In galloanserines, ratites, and crocodilians, the intercarotid anastomosis rests within the hypophyseal fossa and is surrounded (if not within) the cavernous sinus. In all three clades, branches to the hypothalamus are the first to branch off the encephalic arteries. The anatomical arrangement for hypothalamic cooling mechanism via the cavernous sinus occurs then in Crocodylia and most likely all extant birds. Moreover, in birds and crocodilians the cavernous sinus receives blood from the orbital, oculomotor, and trochlear (in crocodilians) vessels, and receives some blood draining from the profundus vein. All of these vessels drain from the various plexuses within the orbit (e.g., the ciliary and choroid plexuses) or have connections with the circumorbital plexuses (e.g., temporal rete, postorbital plexus).

In Rhea, brain temperature remained 1ºC lower than core body temperature during heat stress (Kilgore et al. 1973). The authors hypothesized this temperature difference allowed rheas to maintain a cool brain and to store heat, the latter of which is an important means of reducing water loss. Both Rhea and Struthio (Crawford et al. 1967) have been shown to store heat during exercise. Since cooling does not occur in the neck, the authors assumed that brain cooling occurs via an ophthalmic rete. Additionally, temperature was tested across several sites in the brain, and no significant temperature difference was found between these various sites (i.e., between the neostriatum and the hypothalamus). 177 This doctoral research also identified an ophthalmic rete in specimens of Struthio and

Dromaius, and Elzanowski (1987) illustrated an ophthalmic rete in tinamous. Based on these observations, it appears that an ophthalmic rete likely occurs in all palaeognaths.

In a comparative study (Kilgore et al 1976), hypothalamic temperature was found to be lower than core body temperature across representatives of several neognath clades: the lesser nighthawk, Caprimulgiformes; mallard, Anseriformes; pigeon, Columbiformes; ravens,

Passeriformes; and roadrunner, Cuculiformes. The temperature difference between hypothalamus and the body core varied between species, being as low as 0.8ºC and as high as 1.29ºC. As in the ratite paper (Kilgore et al. 1973) the authors propose that the primary function of brain cooling through the ophthalmic rete is controlled hyperthermia, being the ability to store heat and maintain a cool brain. The benefit of controlled hyperthermia is the prevention of water loss—the brain is cooled without the use of panting, the latter of which cools the brain, but results in water loss, and when body temperature becomes greater than air temperature, the stored heat is lost to the environment.

Kilgore et al. (1979 ) reported that if venous blood flow to the rete is blocked in pigeons, brain temperature becomes higher (by 0.36ºC) than core temperature during heat stress.

Ventilation of the eye in resting pigeons resulted in a decrease in brain temperature, which was related to the corneal vessels that drain into the ophthalmic rete (Pinshow and

Bernstein 1982). Blockage, or vasoconstriction, of the corneal vessels did not result in change in brain temperature. As blood from the buccopharyngeal cavity flows into the rete in parallel to the corneal vessels, the authors concluded that the buccopharyngeal device compensated for the corneal system. 178 The above examples concern research on hypothalamic cooling. Some mammal

researchers (Cabanac 1995, and references therein) have hypothesized, and experimentally

demonstrated, that in various amniotes the arteries supplying the brain, which run on the superficial aspect of brain tissue, transfer heat to the large lake-like dural venous sinuses, resulting in whole brain cooling.

Calliope hummingbirds are amongst the few avian species to lack an ophthalmic rete,

and have only a small plexus in the caudomedial aspect of the orbit between the supraorbital

and ophthalmotemporal arteries (Burgoon et al. 1987). Thus, these birds do not have the

vascular anatomy that is purportedly needed for brain cooling to function. However, the

authors found that during heat stress hypothalamic temperature was kept at least 0.73ºC

lower than core body (= colonic) temperature. The authors concluded that brain cooling

occurs between the encephalic arteries and the cavernous sinus. An odder result of this

study found that during normothermic conditions brain (= hypothalamic) temperatures were consistently kept higher than core temperature.

Both clades of extant archosaurs have anatomies that would allow for whole brain

cooling. In both groups, the dural sinuses are greatly enlarged, especially the massive

occipital sinus lying over the cerebellum, and receive cooled blood from various cooled

venous plexuses and other vascular devices. As mentioned in the results, many dural sinuses

closely appose the major brain arteries (e.g., the dorsal sagittal sinus and the interhemispheric

arteries).

So, archosaurs seem to demonstrate a dual brain cooling system, one using the

cavernous sinus that selectively cools the hypothalamus, and the other using the enlarged

dural sinuses to cool the whole brain. 179 Ophthalmic Rete

Rete mirabile, meaning “wonderful net,” is a term originally used to describe the extensive network or plexus of small blood vessels found at the base of the brain in certain mammals (mainly ruminants and carnivorans), described by Herophilus and Galen (Baker

1979). The system identified in the above two clades (and now recognized as a convergently evolved structure) is now termed the carotid rete mirabile (as it is formed by branches of the internal carotid artery). Similar vascular structures have been identified in various other vertebrate clades. A rete mirabile is best defined as a vascular structure formed by an artery that ramifies into a large number of parallel smaller arteries or capillaries (which reunite into a single artery after leaving the rete), and a vein that ramifies into a series of parallel veins or capillaries, which run between the arterial capillaries (the venous vessels reunite into a single vein upon leaving the rete). The anatomy of the rete mirabile is such that it forms a countercurrent gas or heat exchange system between the arterial and venous systems.

The external ophthalmic rete is a network of small arteries and veins found in the heads of birds that serves as a brain cooling mechanism (Midtgard 1984a). The avian rete (in galloanserines and in ratites) is suspended by an aponeurosis between elements of AME profundus, closely apposed to the medial surface of AME medialis, dorsal to AM caudalis, and dorsolateral to m. pseudotemporalis (thus it rests between elements of the adductor mandibulae externus and internus complexes). The arterial component of the rete is formed by small arterial branches of the profundotemporal artery after it exits the cranioquadrate canal into the temporal space. The profundus artery, that sends off the large supraorbital and ophthalmotemporal arteries, passes dorsal to the retia. 180 The ophthalmotemporal artery has several anastomoses with the orbital artery, an

early branch of the cerebral artery that passes through the hypophyseal fossa along the

cavernous sinus. Rostrodorsally, the ophthalmotemporal artery anastomoses with the

cerebral ophthalmic artery, a branch of the rostral cerebral artery. The supraorbital artery

anastomoses with the ethmoidal artery, the continuing branch of the caudal cerebral artery,

to form the nasal artery (Midtgard 1984a; pers. obs.). Cool venous blood drained from the

face, moist nasal mucosa, oral mucosa, and pharynx, is carried by veins that pass through the

orbit and into the temporal region where they ramify into small branches that form a rete of

venous vessels that run parallel to the arteries. The above arrangement sets up a

countercurrent heat exchange system by which hot arterial blood is cooled by the much

cooler venous blood, which in turn is warmed by the arteries. The system operates by

essentially placing two pipes against each other, each with fluid passing in the opposite

direction from that of the other (countercurrent). One pipe is carrying a hot fluid and the

other is carrying cooler fluid; since heat tends to conduct to areas of lower temperature, the

warmer fluid loses heat and the cooler fluid gains heat by conduction (heat exchange). The

blood flowing through the ophthalmotemporal and supraorbital arteries that are associated

with the rete is in effect cooled, and these arteries then anastomose with vessels supplying the brain, thus cooling the cerebral blood supply and ultimately the brain. Midtgard (1983) described shunts that operate to perfuse the rete at high ambient temperature or to bypass the structure at cooler temperatures.

Vascular Physiological Devices Other than the Ophthalmic Rete

In Anas platyrhynchos, submucosal venous plexuses were identified in the tongue, the

palate, and the nasal cavity (Midtgard 1984a). The venous plexus of the tongue contained 181 thin walled veins with well developed lumina. The veins of the palate and the nasal cavity had irregular lumina and smooth muscle (as in erectile tissue). The arteries were superficial to the veins in the palate and deep to the veins in the nasal cavity.

This study identified similar venous plexuses in the nasal cavity, tongue, and palate in galliforms, ratites, and crocodilians. Moreover, in all of these organisms, the venous plexus of the palate extended caudally into the region of the choana. Galliforms, anseriforms

(Midtgard 1984a), ratites, and crocodilians all exhibited a dense venous plexus associated with the palatal plexus that extended across the pterygoid to form a pterygoid plexus (as in mammals) in the suborbital space.

Additionally, in all groups studied, the large vein of the infraorbital space, the maxillary vein, draining from the palate and dorsal alveolar regions, was surrounded by a dense plexus of long arteries that coursed across and looped around the vein. The plexus consisted of several anastomoses between branches of the “sphenomaxillary,” submandibular, and maxillary arteries. In crocodilians, the only extant archosaur group with a well developed dorsal alveolar canal, the arterial plexus surrounding the dorsal alveolar vein becomes particularly dense in the canal. The veins also ramify into a plexiform system in the dorsal alveolar canal, and the entire vascular bundle of the dorsal alveolar canal takes on a spongy, cavernous tissue appearance that it particularly striking in the paravestibular blood space.

Midtgard (1984a) further identified arteriovenous anastomoses in several region of the duck head. Arteriovenous anastomoses (AVA’s) were found throughout the nasal vestibule. AVA’s were found in the foramina and furrows of the bony rhamphotheca. 182 AVA’s were also found in both palpebrae, and were supplied by branches of the facial,

infraorbital, and supraorbital arteries.

Midtgard (1984a) also found clear differences in the density of AVA’s in the nasal

cavity. The rostral nasal concha possessed, overwhelmingly, the highest AVA density,

followed by the middle concha. The nasal septum, followed by the lateral nasal wall had the

next highest densities, and the caudal concha had a zero density.

Vascular corrosion casts of galliforms demonstrated particularly dense arterial and

venous plexuses in the rostral and middle conchae, and were identical in composition to

corrosion casts of the same area prepared in anseriforms. Additionally, in several places the

vascular connections occurred between blue vessels (venous injected) and red vessels

(arterial injected), and the connecting vessels were purple. Entire areas of these conchae had

a mixed, purple coloration. Of further interest, in all studied galloanserines, the cavernous-

appearing tissue of the casts extended to and filled the soft tissue of the nares, creating a

canal of potentially erectile tissue through which the airstream must travel. The spaces were frequently “lit up” in stereoangiographs of barium injected specimens.

None of the ratite corrosion casts had filling of the areas of the nasal cavity.

However, when cut in section, the rostral and middle conchae of latex injected Struthio demonstrated a highly vascular system of arteries and veins, and the tissue had the typically spongy appearance of narial erectile tissue.

Interconnected Network of Vascular Physiological Devices and the Brain

In birds, the profundus vein, which travels along and drains into the ophthalmic rete, drains through the “middle meningeal” foramen into the sphenotemporal sinus, which ultimately drains into the torcular herophili. The torcular herophili and its drainage 183 system—the occipital sinus and the second confluence of sinuses—can almost completely envelope the dorsal and lateral aspects of the cerebellum and portions of the caudodorsal medulla. In crocodilians and birds, the orbital, trochlear, and oculomotor veins drain into the cavernous sinus. Thus, the veins draining from the orbit can bring cool blood to the sinus that surrounds the hypothalamus, the organ responsible for brain temperature regulation. In birds and crocodilians the trochlear and oculomotor veins, along with the profundus vein, also drain into the sphenotemporal-transverse sinus system. The abducens vein drains into the basilar sinus, which drains and rests across the medulla. In addition to the veins, the orbital arterial system, as discussed in chapter 3 in regard to hormone transport, has extensive connections with the brain’s arterial supply.

In crocodilians, discussed in chapter 3, the temporoorbital artery and vein break up into small, loose plexuses after passing out of the cranioquadrate canal. Similarly, the temporoorbital artery gives rise to the ophthalmic rete after exiting from the cranioquadrate canal. Again, similar to birds, the plexuses of crocodilians are situated within the aponeurotic tissue connecting AMEP pars rostralis and caudalis, and the venous plexus is lateral to the arterial plexus. Thus, the crocodilian temporal plexuses appear to be rudiments of an ophthalmic rete or represent an ancestral precursor to the rete.

In both birds and crocodilians the temporal vascular physiological devices are connected to an extensive and complex plexiform network that extends across the circumorbital rete, supplied by the supraorbital, orbital, and ophthalmotemporal arteries, and connected to the choroidal and ciliary plexuses. Additionally, the lateral components of the circumorbital plexus, and branches of the temporal vessels, interconnect laterally with an extremely dense array of vessels across the lateral surface of the postorbital bone of Alligator 184 and the postorbital ligament of birds, and in both groups the venous plexus is predominantly

lateral to the arterial plexus. Additionally, these last plexuses extend rostrally to interconnect

with the vast lateral periorbital and palpebral plexuses, which are extremely dense in both

groups. Again, Midtgard (1984a) identified AVA’s in both palpebrae of ducks, and the

corrosion casts of galliforms and crocodilians is very similar to those of anseriforms and

demonstrate large “purple” areas where arterial and venous blood are extensively mixed.

The orbit and its ring of periorbital plexuses appear to be an intersection between brain cooling centers and the brain. This research found that in many amniote clades, including archosaurs, there are extensive anastomoses in the orbit, through the ophthalmotemporal venous system and the ophthalmic rete, that link five vascular physiological devices located in different head regions, which likely act as physiological devices that facilitate selective brain temperature regulation. These devices are found in the nasal (nasal vestibular vascular plexus) and oral cavities, the pharynx, and the eye (ciliary and choroid plexuses). All of the devices either directly or indirectly supply blood to the cranial cavity. Additionally, some of these systems form retia with arteries and cool the arterial blood en route to the eye through countercurrent heat exchange. In birds, the antorbital plexus is a sixth, centrally located vascular device. This is a dynamic, interconnected system of vascular devices likely involved in brain temperature regulation.

Related to this system are the external cranial nerve foramina. In archosaurs these

foramina are enormous, and it is difficult to imagine that these foramina accommodate only

nerves. In extant birds and crocodilians enormous veins pass through these foramina into

the cranial cavity. The orbit of extant archosaurs contains a complex array of anastomosing

veins that drain the Harderian gland, eye, eye musculature and receive blood from the 185 various vascular phsyiological devices. The veins of the orbit drain into the dural sinuses, providing a means by which the countercurrent system can effect the brain through anastomosing veins and arteries that drain and supply the brain.

Suborbital Plexus

The antorbital sinus is a paranasal air sinus that communicates with the nasal cavity through an ostium adjacent to the choana (Witmer 1995b). The air sac sits within the antorbital cavity, a bony space partly enclosed by facial bones, but usually open laterally via the external antorbital fenestra. The suborbital diverticulum is an evagination of the antorbital sinus found in birds that extends caudally into the orbit and wraps around the ventral aspect of the eyeball, and interleaves with and is interleaved by the m. pterygoideus dorsalis and the adductor mandibulae musculature (Witmer 1995b).

In nearly all vertebrate animals, the paranasal air sinuses are enclosed within bone and cartilage, as can be seen in the maxillary and frontal air sinuses in humans, and are thus mechanically prevented from expansion; any movement of air in or out of these sinuses is based on diffusion and the air sacs are essentially dead air space. In extant crocodilians, the developmental process of nasal rotation has changed the facial morphology to the extent that the antorbital air sac is no longer laterally open, and is almost completely enclosed in a bony cavity, with the caudal aspect of the sinus in close contact with the rostral aspect of m. pterygoideus dorsalis (Witmer 1992, 1997). Thus, extant crocodilians are specialized archosaurs in that the antorbital air sac is no longer laterally open. In this sense, the crocodilian antorbital sinus is analogous to mammalian sinuses in that they are enclosed within bone and are dead air space (Witmer 1995b). 186 The suborbital diverticulum of birds, however, is a unique structure to vertebrates, in that it is not enclosed by bone, which increases its potential for inflation and deflation, that is, to be actively ventilated (Witmer 1992, 1997). Furthermore, and more interestingly, its anatomical association with the jaw musculature necessitates that the air sac is mechanically acted upon by muscular movement of the jaws to the effect that the air sac acts as a bellows pump (Figure 7). Upon closure of the jaws, the muscles surrounding the air sac squeeze it, pushing any air that had accumulated in the air sac into the antorbital air sac and finally into the nasal cavity. Abduction of the jaws creates negative pressure in the antorbital sinus, which sucks air back into the air sac. This behavior is easily seen in living and dead birds by the bulging in and out of the antorbital air sac through the antorbital fenestra with jaw opening and closure (Witmer 1997).

In galliforms and anseriforms, a particularly dense plexus surrounds the antorbital sinus and extends across the suborbital diverticulum. The venous drainage, as described in detail under the infraorbital section, connects the veins of the plexus to the nasal cavity, orbit, jugular system, and the brain. This structure was not identifiable in any ratite, but this is likely the result of poor vascular filling during injection. Though crocodilians lack a suborbital diverticulum, and the antorbital sinus in enclosed within a cavity, the sinus is extremely vascular.

The equid guttural pouch is a possible analog for the avian suborbital sinus. The guttural pouch is a diverticulum of the pharyngotympanic tube that is found in perissodactyls (the structure has been identified in horses, tapirs, and rhinoceros), and convergently in extant hyracoids, some microchiropterans, and a South American mouse

(Baptiste 1998). Although some carnivorans and artiodactyls cool their hypothalamus via a 187 carotid rete, no such structure exists in perissodactyls. Yet, horses have been experimentally

shown to cool their brain during exercise at temperatures greater than 40ºC. Horses tend to maintain brain temperature 0.6-2.0ºC degrees lower than core body temperature (Baptiste

1998). In horses, thirteen centimeters of the internal carotid artery is exposed along the

surface of the guttural pouch. When the guttural pouch was ventilated with cool, warm, or

100% humidified air, the temperature of the internal carotid artery dropped 0.4-5.0ºC in

cadaverous horses, and 1-3.0ºC in anaesthetized horses (Baptiste 1998). Additionally,

stimulated respiration resulted in a 2-3.0ºC drop in temperature. A follow up study found

that the internal carotid artery was cooled in active horses during trotting and cantering

(Baptiste et al. 2000).

The enclosed antorbital sinus in crocodilians likely results from the nasal rotation

and the development of a secondary palate (see Witmer 1995b, 1997). The antorbital sinus

was not enclosed in non-crocodyliform archosaurs, and the potential did exist for a

diverticulum to extend into the suborbital space. Features in non-avian theropods such as

recesses in the ectopterygoid, squamosal, and the orbital aspect of the lacrimal are potential

correlates for a suborbital diverticulum (Witmer 1997).

Nasal Vestibular Vascular Plexus and Narial Erectile Tissue

Narial erectile tissue is a possibly ubiquitous soft-tissue system in amniotes. Bruner

(1907) described narial erectile tissue in lepidosaurs, which originates at the opening of the

naris and extends throughout the nasal vestibule. The tissue itself is composed of enlarged

capillaries and veins separated by trabeculae formed of smooth muscle fibers and connective

tissue. The erectile tissue is supplied by small arteries from the medial nasal artery that

follow along the vestibule’s median wall accompanied by ramus medialis nasi of the 188 profundus nerve and the medial nasal vein. The erectile tissue is drained by two to three branches, which drain laterally into the sinus lateralis nasi, which then drains into the maxillary vein and lateral nasal vein. Baumel et al. (1983) described erectile tissue in the nasal mucosa of the nasal cavity of pigeons with “beaded veins” that possess thick muscular walls and arteriovenous anastomoses (AVA’s) that carry blood into them. Bang (1964, 1971) illustrates “areas of heavy blood vascular concentration” in the middle and rostral conchae of cathartid vultures and caprimulgiforms. Bang and Wenzel (1985) further discussed the rostral concha as a highly vascular and important baffling-warming structure in many birds, but which is absent in Dromaius, Gyps, and Pelecanus . It is not known whether any of these morphologies described by Bang actually correspond to erectile tissue.

Recently, studies focusing on crocodilian nasal anatomy have provided more in depth information on crocodilian narial erectile tissue (Bellairs and Shute 1953; Witmer

1995b; Witmer and Sampson in prep.). In a paper describing the narial musculature of crocodilians, Bellairs and Shute (1953) noted the presence of erectile tissue between the cupola and the rostral part of the nasal sac. Witmer (1995b) described a neurovascular bundle containing the rostral dorsal alveolar branch of the maxillary nerve and accompanying vessels (the “internal maxillary vessels” of Hochstetter 1906). In known alligatorids, these vessels enter a foramen lateral to the dorsolateral aperture of the caviconchal recess, run through the caviconchal recess, enter a bony canal located dorsolateral to the postvestibular space, and then pass into the premaxillary vascular space

(the paravestibular blood space). However, these branches of the rostral dorsal alveolar artery pass entirely through a bony canal in Crocodylus. Witmer and Sampson (in prep.) describe three cavernous tissue masses in Gavialis. The first is probably homologous to other 189 crocodilians, being intracapsular and located in the rostromedial portion of the narial fossa.

This first mass is supplied by an intracapsular artery flanked by multiple veins. The second

mass is located external to the cartilaginous capsule and adjacent to the premaxilla. Vessels

passing from rostroventral foramina in the premaxilla supply the second mass. The third

mass is found in the core of the postnarial muscular cushion and is supplied by three

sources: (1) extracapsular vessels running with the nasal gland and n. ramus lateralis nasi; (2) the intracapsular vessel supplying the first mass of erectile tissue; and (3) a large median vascular space located between the contralateral masses of postnarial cavernous tissue.

Chapter 3 elaborates further on the blood supply to crocodilian narial erectile tissue.

Extensive research has been conducted on narial erectile tissue in humans. Human

narial erectile tissue is found in the ventral concha (especially the posterior third of this

concha), occupying most of the width of the lamina propria (Grevers 1994). Capillaries deep to the mucosal epithelium are fenestrated (fenestrations face the adjacent epithelial cells for endonasal fluid exchange) whereas those from the lamina propria have a continuous endothelium, a basal lamina, and pericytes (Grevers 1989, 1993; Grevers and Hermann

1987). Cavernous veins drain the capillary bed and a system of arteriovenous anastomoses

(characterized by vessels with a muscular media and short thickened cells that form a sphincter) (Cauna and Cauna 1973). Intervascular smooth muscle bundles (IMFs) link different areas of the cavernous tissue running parallel to the swell bodies bridge vessels by

inserting into the external muscular coat (Grevers and Kamargakis 1995). Muscular

bolsters, structures that protrude into the lumen of vessels at the transition between two

vessels, and other locations in the cavernous tissue are continuous with the general muscular

lining of the vessels and like the IMFs, contain basic smooth muscle cytoplasmic 190 components. Grevers and Kamargakis (1995) hypothesize these bolsters to be contractile

elements.

Dawes and Prichard (1953) described very similar cavernous tissue morphologies in the nasal cavities of other mammals (dogs, cats, rabbits, rats, goats, sheep, and pigs). The most highly vascularized areas of the nasal cavity were the mucosa associated with the maxilloturbinates and nasoturbinates, mucosal regions that are amongst the most exposed regions of the nasal cavity to inspired air. In dogs, cats, and rabbits, this nasal mucosa was shown to have extensive arteriovenous anastomoses, characterized by vessels with thick muscular walls and no internal elastic lamina. Furthermore, the dense vasculature of the nasal mucosa contains thick-walled veins and venules as is found in human erectile tissue.

When open, the arteriovenous anastomoses are hypothesized to divert blood flow from the glandular capillary plexus. The arteriovenous anastomotic vessels are further characterized by shunts that can reduce the total blood flow into the subepithelial capillary plexus.

Moreover, the thick muscular walls of the above mentioned veins can act as a sphincter, which would prevent blood from leaving the cavernous tissue. The combined action of the

AVA’s diverting blood into the erectile tissue away from the capillary beds of the mucosa, and the action of the muscular veins and venules in preventing this blood from leaving the cavernous tissue, is responsible for the swelling of the organ. Through the action of erection and deflation, the cavernous tissue appears to control the circulation through the capillary beds of the nasal cavity. The superficial, subepithelial capillary plexus is considered to be the main source for warming inspired air, but this is thought to be a less important function of the plexus than its involvement in moistening the inspired air (Dawes and

Prichard 1953). Changes in the blood flow through the glandular capillaries indirectly affects 191 the humidification of inspired air through the capillary bed’s influence on the viscosity of the

mucous blanket, secreted by the mucosal glands, which provides the actual moisture that

humidifies the inspired air. Thus, by regulating the amount of blood that passes through the

subepithelial and glandular capillary beds, the nasal cavernous tissue actually regulates the

humidification and warming of inspired air on two levels.

In humans, it has long been noted that there exists at any one time a unilateral nasal

obstruction, which results from the erection of the cavernous tissue associated with the

inferior concha (Principato and Ozenberger 1970). The unilateral obstruction follows a

cyclical pattern with obstruction of one side of the nasal cavity lasting 3.5 hours on average in humans, this phenomenon has been termed the nasal cycle.

Bojsen-Møller and Fahrenkrug (1971) described a similar cycle in rats, rabbits, and

cats. In cats the cavernous tissue is associated with the septum and the vestibular

component of the maxilloturbinal; in rats, cavernous tissues (“swell bodies”) were found

only in and around the internal ostium between the naso- and maxilloturbinals; in rabbits

cavernous tissue was found on the medial aspect of the unbranched portion of the

maxilloturbinal and the septum, whereas venous sinuses were found throughout the

branched portion of the maxilloturbinal. In the rat, the excretory ducts of the rostral nasal

gland, which drain acini from the wall of the maxillary sinus, pass through the cavernous

tissue, and the largest duct was found to be compressed against the side of the nose when

the erectile tissue became distended. In all of these animals, the cavernous tissue was more

concentrated in the ventral component of the respiratory passage leading to the nasopharynx

(e.g., the internal ostium) than it was in the olfactory portion of the nasal cavity. The authors

present a model of the nose as actually a system of two parallel, but separate respiratory air 192 passages, which cyclically alternate. The authors emphasize that any attempt to understand the function of the nasal cavity in heat exchange and water recovery must take into account its periodicity. The mucosal surface of the more conductive air passage will experience greater cooling, and thus greater heat and water recovery, over the non-patent side.

Moreover, increased evaporation of water will alter the mucous viscosity, and in turn affect ciliary action, which as discussed above affects humidification of inspired air.

Ritter (1971) emphasized that the nasal cycle varies both heat loss and mucous production, and as such regulates humidification, and warming of the inspired air as needed by the organism. Beickert (1951) demonstrated a rhythmic alternation in tonus of the autonomic nervous system from one side of the head and neck to the next, which affects the nasal cycle, lacrimal and nasal secretion, vessel diameter size in the conjunctiva, and changes in pupil size (Bojsen-Møller and Fahrenkrug 1971). Ritter (1971) showed that the cavernous tissue associated with the inferior turbinate of humans experiences rostral vasoconstriction due to sympathetic innervation; however, the caudal aspect of the turbinate has a compensatory dilation of the cavernous tissue due to a parasympathetic response.

Sympathetic vasoconstriction results as a response to increased exercise, whereas the parasympathetics respond at this point with increased nasal mucous production and secretion (thus increasing the ability to humidify inspired air). Tatum (1923) demonstrated

changes in the venous tissue resulting from alterations in temperature, humidity, and Pco2 content of the inspired air.

This paper has briefly proposed, based on gross morphological observations, hypothetical pathways for the autonomic system to various vascular physiological devices and to glands that effect important behaviors, cycles, and physiological mechanisms by 193 secreting various hormones into the cephalic blood vascular system. Several studies have

reported on the anatomy and biological significance of autonomic nervous system-head

vasculature relationships in mammals. Though a few of these studies have examined birds,

very few have looked at crocodilians and other non-avian sauropsids.

Eccles and Lee (1981) determined vasomotor activity in the nasal cavity (e.g.,

mucosal swelling, the nasal cycle) was controlled by a central respiratory oscillator, and that

hyperventilation eliminated such activity. In a series of subsequent papers, Eccles and

various co-authors elaborated on this mechanism and its physiological implications (e.g.,

brain cooling, respiratory defense). Nasal centers in the brainstem, that ultimately regulate nasal airflow, were entrained to an endogenous rhythm controlled by the hypothalamus

(Flanagan and Eccles 1997 ). Bilateral nasal constriction resulted from stimulation of the hypothalamus (Flanagan and Eccles 1991 ), which regulated sympathetic innervation to structures of the nasal cavity (Eccles and Lee 1981).

The sympathetic oscillators responsible for the nasal vasomotor oscillation were

entrained by respiratory activity. Vasoconstriction and mucosal shrinkage occurred during inspiration, and vasodilation and mucosal swelling occurred during expiration. However, in accordance with the nasal cycle, one nasal passage would exhibit a higher oscillation in response to stimulation of the reticular formation in the brainstem, and the nasal oscillators demonstrated reciprocal inhibition (Bamford and Eccles 1982). Importantly, the nasal mucosa in the nasal passage with the lowest resistance maintained vasomotor and secretory activity which conditioned the inspired air.

Bamford and Eccles (1983) demonstrated a direct effect of this system on brain

temperature regulation. Brain cooling was inhibited by bilateral stimulation of the superior 194 cervical ganglion, which was found to effect nasal air flow and blood flow in the nasal

mucosa in domestic ducks. In amniotes characterized by well developed arterial retia in the

nasal cavity (Felis, Sus, Anas), brain cooling was regulated via control of blood flow through the nasal mucosa. Pertinent to this study, control of nasal blood flood in Anas platyrhynchos was exerted by the sympathetic system, that, as in mammals, induced vasoconstriction and shrinkage of the nasal mucosa. Under normal conditions, ducks maintained a brain temperature 1-2ºC lower than the core body temperature. There was a decrease in air resistance with stimulation of the superior cervical ganglion, and an increase in brain temperature. Air pulsed through the choanae resulted in a decrease in brain temperature approximately 15-30s after the air flow onset However, no cooling occurred if the brain temperature was already low (38.5ºC) before the onset of air flow. Even under conditions of pulsed air flow, convective cooling of the brain was eliminated by stimulation of the sympathetic innervation, and brain temperature increased by as much as 0.5ºC. Brain temperature would again decrease after sympathetic stimulation ended. Bamford and Eccles

(1983) further implicated the pharynx and facial skin, all of which were drained by veins that ultimately come in contact with the cerebral carotid artery, as possible brain cooling devices.

Stimulation of the internal carotid nerve (containing postganglionic sympathetic fibers from the superior cervical ganglion) in Felis resulted in contraction of the nictitating membrane, and vasoconstriction of vessels in the tongue and arterioles and venous sinusoids in the nasal mucosa (Eccles and Wallis 1976 ). As in extant archosaurs, the cat tongue contains a dense vascular plexus.

In addition to their importance in brain cooling, Eccles (1996) showed that, in mammals, the venous sinusoids of the nasal erectile tissues produce plasma exudates, and act 195 as an early respiratory defense mechanism. The decongestion and congestion of these sinusoids create a pump that generates the plasma exudates. During decongestion, the sinusoids contract from increased sympathetic tone and squeeze out plasma that then passes through the fenestrated endothelium. During congestion the sinusoid become greatly distended, which stretches the smooth muscle surrounding the sinusoids, which then

“unzips” the tight cellular junctions, thus increasing permeability and resulting in the exudation of plasma onto nasal cavity epithelium. The nasal cycle has been found to increase during respiratory tract infection (Eccles et al. 1996). This system has been studied in euarchontoglirines (primates and glires) and has apparently not been explored in archosaurs or any other amniote group.

In euarchontoglirines, air flow resistance through a nasal passage is regulated by exercise and posture, in addition to the respiration-linked autonomic innervation of the veins of the nasal erectile tissue. Sympathetic tone increases during exercise, which decreases airflow resistance and increases nasal vasoconstriction (Richardson and Seebohm 1968).

Also, the vessels of the nasal mucosa have a dense number of adrenergic receptors, and vasoconstriction in the nasal mucosa increases with high levels of circulating adrenaline in the blood plasma, decreasing airway resistance in the nasal cavity (Malcolmson 1959).

Though extant avesuchians do not possess a vomeronasal organ, nasal erectile tissue is an important component of the vomeronasal complex in many amniotes.

Though narial erectile tissue has been identified outside of Mammalia, it is not known if these organisms experience anything like a nasal cycle or if the nasal cavernous tissue is related to heat exchange and water economy by regulating nasal blood flow.

Additionally, based upon the extensive arteriovenous anastomoses, the venous morphology, 196 and the close proximity of arteries and veins, one would expect the cavernous tissue itself to

be a countercurrent heat exchanger (Baumel 1983). A dramatic reduction in heat from the

canine penis (an erectile tissue based organ) was found when the prepuce was withdrawn

(Ninomiya and Nakamura 1981). However, no researcher has attempted to elucidate

whether or not the nasal erectile tissues acts as countercurrent heat (or gas) exchangers in

any animal.

As mentioned above, cephalic vascular structures have been elaborated into brain

cooling devices in various amniote clades (e.g., in birds Richards 1970; Kilgore et al. 1973,

1976; Bech and Midtgard 1981; Arad et al. 1988, 1989). Though brain cooling has

traditionally been considered an important mechanism to protect against neural tissue

damage (see Ghoshal 1985), recent studies suggest that , at least in mammals, brain cooling

acts as a signal to the hypothalamus to regulate water loss during heat stress (see Jessen

1999). This study has already identified several dense vascular structures in crocodilians that

seem to correspond with avian retia involved in brain cooling. Spotila et al. (1977) found the

head of crocodilians to be significantly cooler than the body during heat stress, but

concluded by stating, “the mechanisms by which heat is transferred from the brain region to the mouth where it is dissipated during cooling are not known at present.” This research provides the opportunity to answer this question by determining the vascular structures responsible for the heat dissipation. In addition to and associated with brain cooling structures, narial vascular erectile tissues have been implicated in several important physiological processes, including the formation and secretion of nasal plasma exudates as a first line of respiratory defense (Eccles 1996); the release of gonadotropin-releasing hormone from the vomeronasal organ (Døving and Trotier 1998); water reclamation (Dawes and 197 Pritchard 1953); and in the obstruction of the respiratory pathway during the nasal cycle

(Bojsen-Møller and Fahrenkrug 1971). An important component of this research will be a comparative study of such narial erectile tissues in archosaurs and other amniotes. Recently, several dense vascular plexuses in the mammalian pharynx have been found to constrict the respiratory passageway and control the respiratory airstream (Wasicko et al. 1990). Evidence from this current study has determined similar vascular arrangements in the pharyngeal regions of extant archosaurs.

Vessels of the Nasal Vestibular Vascular Plexus

The nasal vestibular vascular plexus (hereon the NVVP) in amniotes is comprised of six major blood vessels: the palatine, dorsal alveolar, premaxillary, lateral nasal, medial nasal, and sphenopalatine arteries. Figure 8 depicts the NVVP in extant diapsids. All of these vessels have osteological correlates, many of which are identifiable in fossil taxa. The following list briefly discusses each vessel and their osteological correlates.

(1) Palatine artery—The palatine artery exits the orbit and enters the ventral palatal region via the rostral aspect of the suborbital fenestra (in basal sauropsids such as turtles, it pierces a foramen in the palatine bone). The vessel often gives off caudoventral pharyngeal branches.

In crocodilians and some fossil archosaur species, the palatine artery sends branches into the dorsal alveolar canal via a longitudinal series of foramina along the medial aspect of the tooth row to anastomose with the dorsal alveolar arery. The palatine artery continues to pass along the ventrolateral palatal surface and often anastomoses with the dorsal alveolar artery through foramina in the maxilla. In all studied amniotes the vessel enters the vestibular region through a foramen in the premaxilla (the nasopalatine artery of mammals) near the maxilla-premaxilla suture to join the vestibular vascular plexus, and anastomoses 198 with branches of the lateral nasal artery. In birds, the palatine artery is typically a remnant, termed the lateral palatine artery, that travels along the ventrolateral surface of the maxilla and forms the lateral palatine plexus. In neognaths, the vessel does not anastomose with the dorsal alveolar artery, probably due to loss of the alveolar process of the maxilla. As mentioned in the results section, the ratite supply to the palate is very similar to crocodilians and differs from that of neognaths. Ratites do not reduce the maxilla to the extent most other birds do, and foramina along the ventral maxilla allow the palatine artery to anastomose with the dorsal alveolar artery. In Neoaves, the major supply of the avian palate derives from a single median vessel, the median palatine artery, that forms by the anastomosis of the medial palatine arteries, themselves ultimately branches of the oromandibular artery, whereas the median palatine artery is formed by the anastomosis of the terminal branches of the dorsal alveolar artery in ratites. Interestingly, in birds, the median palatine artery sends off dorsal branches into the nasal cavity that anastomose with the medial nasal arteries through the soft tissue medial to the premaxilla-maxilla suture.

(2) Dorsal alveolar artery—The dorsal alveolar artery passes through a neurovascular canal

(the mammalian infraorbital canal) in the maxilla (entering through a foramen in the rostrolateral aspect of the infraorbital space) with the maxillary nerve to run medially against the bone. The artery ramifies into a multitude of branches, some of which supply teeth, the paranasal sinuses (in crocodilians and mammals), the perichoanal region, and the skin through nutrient foramina. In non-mammalian synapsids and non-avian sauropsids, the dorsal alveolar artery exits the canal into the nasal vestibule through a foramen near the premaxilla-maxilla suture to join the nasal vestibular vascular plexus, often by anastomosing with the lateral nasal artery. In most non-avian and non-crocodilian archosaurs, the dosal 199 alveolar canal opens medially into the caudolateral nasal vestibule through a foramen rostromedial to the premaxillary process of the maxilla. In crocodilians the vessel opens medially after anastomosing with the palatine artery into the nasal vestibule through a foramen in the premaxilla, termed here the medial “subnarial” foramen, just rostral to the premaxilla-maxilla suture, after which it anastomoses with the lateral nasal artery. Thus, the medial “subnarial” foramen is similar, if not homologous, to the rostral opening of the dorsal alveolar foramen in other amniotes. A terminal branch of the dorsal alveolar artery in crocodiles enters the premaxilla as the premaxillary artery. In ratites the dorsal alveolar artery enters small nutrient foramina in the maxilla, and its main branch passes dorsal to the maxilla and then splits through a foramen in the maxilla to pass on the ventral rhamphothecal aspect where it then enters the premaxilla through small caudoventral foramina. As in other amniotes, the ratite dorsal alveolar artery sends off lateral branches that pass to the rostral facial surface via nutrient foramina. In neognaths the dorsal alveolar artery is greatly reduced, and in anseriforms the vessel and its ancestral supply pathway is replaced by a branch of the submandibular + pterygoid arterial anastomosis.

(3) Premaxillary artery—The premaxillary arteries are terminal branches of the dorsal alveolar artery in archosaurs, which run rostrally and then medially through the premaxilla forming large blood spaces in crocodiles. Branches of this vessel pass through foramina in the premaxilla to run caudoventrally through the submucosa of the solum nasi and anastomose with the medial nasal artery, and the “sphenopalatine artery.”

(4) Medial nasal artery—In all studied amniotes, the medial nasal artery travels rostroventrally across the nasal septum, sending off branches to the nasal concha, and eventually passing throught the submucosa of the solum nasi where it anastomoses with other branches of the 200 NVVP. See results in Chapters 2 and 3 for further information about this vessel and its field of supply. The medial nasal artery has no clear osteological correlate. However, the artery is associated with the nasal septum, and forms a plexus across it in all extant amniotes studied.

The artery supplies the erectile tissue of the conchae in birds, the cavernous conchal tissue in mammals, and the ventral component of the narial erectile tissue of crocodilians.

(5) Lateral nasal artery—The lateral nasal artery travels as an extracapsular vessel that eventually anastomses with the dorsal alveolar artery in crocodilians and non-avian amniotes

(see Witmer 1995b and the results section for more information). The lateral nasal neurovascular bundle travels with the nasal gland in archosaurs and the complex grooves the nasal bone (Witmer 1995b). The artery supplies the rostral and lateral aspects of the narial erectile tissue of crocodilians and the cavernous conchal tissue in mammals.

(6) Sphenopalatine artery—The sphenopalatine artery travels with the ventral branch of the palatine ramus of the facial nerve. The vessel and nerve are associated with the blood supply to the erectile “mushroom” body in some mammals and lepidosaurs. In crocodilians the vessel runs through the solum nasi toward the erectile tissue mass, and in birds the vessel anastomoses with branches of the medial nasal artery along the caudoventral nasal septum.

The vessel has clear osteological correlates in extant and extinct archosaurs (and many other amniotes: the “pterygoid” canal) that are discussed in the discussion section of Chapter 3. 201

CHAPTER 3

CEPHALIC VASCULATURE IN ARCHOSAURIA II: CROCODYLIA, WITH

SPECIAL REFERENCE TO ALLIGATOR MISSISSIPPIENSIS

INTRODUCTION

The vertebrate head is a dynamic assemblage of complex interacting functional units.

It is unique within the body in that it represents the point of intersection of the digestive, neural, endocrine, respiratory, sensory, and other systems that directly determine an organism’s survival and reproductive success. Understanding cephalic structure and patterning, as well as the interaction of its functional units, is fundamental to understanding the macroevolutionary history of amniotes. In the past century morphologists have greatly furthered our understanding of the histology, anatomy, physiology, development, biomechanics, and evolutionary history of several cephalic anatomical systems. Extensively researched systems and functional units in the vertebrae head include the skull (e.g., De Beer

1937; Hanken and Hall 1993), chondrocranium (e.g., Bellairs and Kamal 1981, for non-avian sauropsids), head musculature (e.g., Edgworth 1935; and see Shwenck (2000) for a current review of jaw musculature), the eye (e.g., Walls 1942), the nose (e.g., Negus 1958), and neuroanatomy (e.g., Butler and Hodos 1996). Many of these studies have been comparative and have attempted, where possible, to identify homologous structures. In light of these achievements, it is surprising that the vascular supply to the craniofacial regions of vertebrates, well recognized as an intrinsically important component of the vertebrate head, has been a relatively neglected system. 202 Similarly, just as vasculature has often been ignored as a topic of comparative

anatomical research, Crocodylia has been a frequently ignored vertebrate clade. However, in

a deep time perspective, Crocodylia is an incredibly important clade for any proper

understanding of terrestrial vertebrate history. Along with birds, the volant descendents of

theropod dinosaurs, crocodilians are the only living representatives of the

Archosauromorpha, a clade that included non-avian dinosaurs, pterosaurs, most of the

incredible diversity of marine reptiles (placodonts, ichthyosaurs, plesiosaurs) (Merck 1997),

and a host of bizarre basal forms (including protorosaurs, phytosaurs, aetosaurs, and

rhynchosaurs). Together, the diversity of form and behavior ecology exhibited by the

Archosauromorpha must have rivaled if not exceeded that of extant Mammalia. As birds

and crocodilians are the only living archosauromorphs, they provide us with the best means

to reconstruct a large component of the biological history of vertebrates over a time scale of

three hundred million years.

The recent use of the extant phylogenetic bracket approach has proved an extremely

useful methodological tool for reconstructing the evolution of the archosaurian head

(Witmer 1995b, 1995b, 1997, 1998; Papp and Witmer 1998; Sampson and Witmer 1999;

Sedlmayr and Witmer, 1998, 1999). Witmer (1995b) has emphasized the importance of reconstructing soft tissues (such as vasculature) in fossils for three main reasons: (1) the role of soft tissues in the existence, maintenance, and structure of bones; (2) the importance and role of soft tissues in paleobiological inferences; and (3) the use of soft-tissue relationships to

systematists in making hypotheses on the independence and non independence of

phylogenetic characters. 203 However, the reconstruction of soft tissues in archosaur heads is complicated because both extant archosaurian clades have highly apomorphic head morphologies, a fact that makes difficult any attempt to homologize cephalic structures and infer evolutionary history for Archosauria. Any comparative study of archosaurian cephalic vasculature must take the radical differences between birds and crocodiles into consideration. In birds, the great enlargement of the eye and brain (Coulombre and Crelin 1958, Witmer 1995b), and extensive bone loss, fusion, and reduction, should all effect avian cephalic vasculature. In many ways, the crocodilian head is even more derived from the basal archosaurian condition.

In the course of development and evolution, the crocodilian head has experienced fusion of the quadrate and pterygoid to the braincase, nasal rotation (Witmer 1995b), a secondary palate (Ferguson 1981, 1984), and basicranial metamorphosis (Tarsitano 1985). It was expected that these complex changes would have greatly effected the head vasculature, and is for this reason that the most surprising result of this study is the discovery of great similarities between the cephalic vascular systems of birds and crocodilians.

Biological Importance of Head Vasculature Cephalic vasculature is an important system that contributes to an organism’s biology in a variety of ways. (1) Vascular structures and patterns can have major effects on the structure, patterning, and development of other anatomical systems including the bony skull

(see Hopson [1979] for specific effects of the dural venous sinuses on the skull, Witmer

[1995b], Geisler and Luo [1998]). In discussing the development of limb vasculature,

Feinburg (1991) emphasized that vasculature both contributes and responds to morphogenesis and cytodifferentiation through epithelial-mesenchymal interactions, cell- matrix interactions, and programmed vascular regression that helps model the skeleton. 204 Such interactions are likely to occur in the developing head, as well. (2) Blood vessels, along

with nerves, have often been critical in determining the homologies of skeletal elements

among different amniote clades (Presley 1993). (3) Cephalic vasculature is the exclusive

source of nutrient supply and gas exchange for cephalic tissues. (4) Cephalic arteries and

veins can form countercurrent heat exchangers, which can be critical in water economy and

cooling or warming different tissues (e.g., brain cooling [see Ghoshal 1985]; evaporative

cooling of the head [Arad et al.1989]). (5) Vascular structures can increase the amount of

oxygen delivered to a tissue via countercurrent gas exchangers (e.g., the use of the

ophthalmic rete to increase the brain’s oxygen supply at high altitudes in birds [Bernstein et al. 1984; Pinshow et al. 1985]). (6) Cephalic vessels can contribute to morphological units that have mechanical functions (e.g., the closing of the nasal air passage via narial erectile tissue [Bojsen-Møller and Fahrenkrug 1971, Witmer and Sampson, in prep.]; erection of the

vomeronasal cavernous tissue as the mechanical force underlying secretion of

gonadotropin-releasing hormone from the vomeronasal organ [Døving and Trotier 1998]).

(7) Cephalic vessels can be elaborated into behavioral display devices (e.g., the wattles and

combs found in birds are composed of dense arteriovenous anastomoses and capillary beds

[Lucas and Stettenheim 1972]).

Previous Research Previous research on crocodilians—all of which is at least 85 years old—includes a

discussion of the vascular supply to the tympanic cavity and brain in Crocodylus acutus (Owen

1850), brief discussion of the cephalic vasculature in Alligator mississippiensis (Reese 1914), the

embryological development of the vasculature in Crocodylus (Hochstetter 1906; Shiino 1914),

and the major trunks of the dorsal carotid artery (Shindo 1914). 205 Organization of the Paper As in Chapter 2, the results section of this paper is organized in a caudal to rostral

descriptive pattern, following the pattern of arterial flow. The distal common carotid artery

and its proximal branches are discussed first, and the blood supply to the dermis of the

rostrum is discussed last. Following the format of the second chapter, vessels are discussed

in reference to anatomical regions (e.g., the nasal cavity and orbit), with an emphasis placed

on anatomical interrelationships. For each anatomical region, a detailed account will be

given for the vessels and their branches, including the structures the vessels supply or drain.

The discussion will focus on the evolution of the crocodilian head and the (few) differences

between avian and crocodilian head vasculature. The discussion will then address

buccopharyngeal vascular physiological devices in archosaurs, and finally offer a hypothesis of the orbital vasculature as an important transport mechanism for physiologically and behaviorally important Harderian gland secretions.

Materials and Methods

Taxa Studied All of the following specimens used for this study were obtained as preserved or fresh heads

or whole animals: (1) 19 Alligator mississippiensis, (2) 5 Caiman crocodylus, (3) 5 Crocodylus

sianensis, (4) 4 Crocodylus novaeguineae, (5) 4 Crocodylus porosus, (6) 1 Tomistoma schegelii , (7) 2

Gavialis gangeticus, (8) 2 Iguana iguana. Alligator mississippiensis specimens were acquired from the Rockefeller Wildlife Refuge, Grand Chenier, LA., and specimens of Caiman crocodylus and

Crocodylus siamensis were acquired from St. Augustine Alligator Farm, St. Augustine, FL. C. novaeguineae and C. porosus specimens were acquired from a crocodile farm in Papua New

Guinea. The Tomistoma and one Gavialis specimens were both embryonic, un-numbered, specimens on loan from the Smithsonian Museum. The second Gavialis specimen consisted 206 of a snout and was studied by Witmer and Scott Sampson (Witmer and Sampson, in prep.) at

the Madras Crocodile Bank, India. Numerous dried skulls of the above taxa and of

Paleosuchus palpebrosus (OUVC 9602) were studied from the Ohio University Vertebrate

Collections (OUVC). Additionally, bony skulls of A. mississippiensis, C. novaeguineae, and C.

porosus from various embryological stages in the OUVC were studied.

Fossil skull material from the following extinct archosaurs were also studied,

Proganochelys quenstedti (SMNS 16980), Mesosuchus (SAM 6536), Stanaelorhynchus stuckleyi

(University of Tübingen, uncataloged), Scaphonyx (University of Tübingen, uncataloged),

Proterosuchus (NMQR 880), Erythrosuchus africanus (BMNH R3592, BPI 18893), Euparkeria capensis (UMZC T692, SAM 5867, 5876, 6050, 7696, 7996), Rutiodon adamensis (type, UCMP

27181 V 7034, UCMP 34250 V 2816), Ornthosuchus woodwardi (BMNH R3142), Phytosaurus

kapfii (BMNH 38037), Batrachotomus kupferzellensis (SMNS 52970), Teratosaurus suevicus

(BMNH 38646, R 29112), Stagonolepis (BMNH), Desmatosuchus haploceras (UCMP 27404

A269), Sphenosuchus acutus (SAM 3014), Baroqueosuchus (BPI 4946), undescribed crocodylomorph (UCMP 97638 V 6899), Protosuchus richardsoni (UCMP 130860 V 84246,

UCMP 131827 V 85012, 138843 A269), Orthosuchus (SAM K409, K4639), Pelagosaurus

(BMNH 36200), Metriosuchus moreli (BMNH R 3900), Brachychampsa montana (UCMP 133901),

Borealosuchus sternbergi (UCMP 130767 V 88047, UCMP 138375 V 88047), Gryposuchus (UCMP

V), Hylaeochampsa (BMNH R177), Asiatosuchus (SMNK 2351), Eogavialis (BMNH R 3108, R

3195, R 3199, R 3337, R 3425, R 3430, R 3433, R 4332), Diplocynodon hantoniensis (BMNH

3092, 3096, 30287, 30393), “Crocodylus” megarhinus (BMNH R 3327, R 3328, R 3104),

Crocodylus robustus (BMNH R 2193), Crocodylus lloydi (BMNH 83333), Crocodylus paleoindicus

(BNNH 39797, 39797, 39799), Tapejara (SMNK, uncataloged), Hypsilophodon foxii (BMNH R 207 197, R2477), Dryosaurus (University of Tübingen, uncataloged), Plateosaurus (University of

Tübingen, uncataloged).

Institutional abbreviations: BPI, Bernard Price Institute, Johannesburg; BMNH, Natural History

Museum, London; NMQR, Bloemfontein National Museum; SAM, South African Museum,

Cape Town; SMNK, Staatliches Museum für Naturkunde Karlsruhe; SMNS, Staatliches

Museum für Naturkunde Stuttgart, Federal Republic of Germany; UCMP, University of

California Museum of Paleontology, Berkeley; UMZC, University Museum of Zoology,

Cambridge

Figure 4C is a cladogram depicting the relationships of the organisms used for and

discussed in this paper, and demonstrating their positions within Archosauromorpha. Figure

9 is a cladogram of Crocodylomorpha and the phylogenetic relationships of the crocodilian

taxa studied.

Note on Nomenclature: As birds are the extant sister group of Crocodylia and there is no

standardized nomenclature for either crocodilians or sauropsids, anatomical nomenclature in

this paper follows the Nomina Anatomica Avium (1993). A major purpose of this paper is the

identification of homologous traits with an eye toward establishing homologies in cephalic vascular structures for all of Amniota, and a common nomenclature for homologous structures is considered more pragmatic and less confusing

Vascular Injection The following taxa were prepared by vascular injection: 13 Alligator mississippiensis, 5

Caiman crocodylus, 5 Crocodylus siamensis, 1 Crocodylus novaeguineae, and 1 Crocodylus porosus. All of

the specimens were injected at a juvenile stages of development with the exception of C.

novaeguineae and C. porosus which were adults. 208 The injection apparatus consisted of 18 gauge Hamilton blunt-ended cannulae

(Hamilton Company, Reno, NV) and B-D syringes with Luer-Lok tips (Becton Dickinson

and Co., Franklin Lakes, NJ). Ethicon (Cincinnati, OH) 4-0 Silk suture was sometimes used to ligate cannulated vessels.

For all injections, dissecting scissors were used to make an opening ¼ to ¾ across the vessel, and a blunt-ended cannula was then inserted into the lumen and pushed as far cranially through the vessel as possible. The cannula was kept within the vessel by tying ligature around, or by simply clamping hemostats on, the area of the vessel containing the cannula.

Vascular Corrosion Casting In the course of the study, the following specimens were prepared as vascular corrosion casts: 5 Alligator mississippiensis, 5 Caiman crocodylus, and 5 Crocodylus siamensis.

The purpose of the vascular corrosion cast was to produce a detailed cast of the cephalic arterial system without other soft tissues. Most casts were produced with an intact bony skull, to provide context in interpretation of the vasculature, and to better represent vascular relationships to the skull and determine osteological correlates for vascular structures. Additionally, vascular corrosion casts provided unique insight into complex vascular systems and structures, including the anatomy, composition, and anastomotic relations of vascular plexuses and retia.

Following the above vascular injection protocol, both of the common carotid arteries were injected with Batson’s no. 17 poliester resin (Polysciences, Inc., Warrington,

PA), color red. Blue resin was injected into both jugular veins. After injection, the specimen 209 was immediately placed in a cold-water bath and left for twelve hours to allow the medium to set up.

A 30-40% potassium hydroxide (KOH) or sodium hydroxide (NaOH) aqueous solution was measured out in a beaker. The solution volume (about 1200 ml for a 12 cm long juvenile Alligator head) and beaker size was selected to fully submerge and contain the specimen. The beaker containing the solution was then placed in a water bath (Fisher

Tissue Prep Flotation Bath, Model 134, Fisher Scientific Co., Pittsburgh, PA), and the solution was heated to 37º C. The specimen was then placed into the heated solution and closely monitored throughout the digestive process. Occasionally, the specimen was carefully removed from the solution using a fine mesh net or large forceps, placed upon a tray, and then mechanically prepared using a thin jet of water and fine point forceps.

Mechanical preparation was used to remove muscle and other soft tissues from the bone with little damage to the vascular cast. The specimen was fully removed from the solution after a one to four hour period, dependent upon the extent of the soft tissue digestion and the preservation of the bony skull. The specimen was then rinsed in water for half an hour, and then placed in a 10% hydrogen peroxide, 30% ammonia, aqueous solution for one hour.

The specimen was then rinsed in water for another half hour. After being removed from water, the specimen was set out to dry over a twelve-hour period. Forceps were used for subsequent pruning of excess vessels, and for dissection of the cast, under a light dissecting microscope (Nikon Stereoscopic Microscope SMZ-U, Nikon Corporation, Tokyo, Japan). 210 Gross Dissection Vascular injected heads of Alligator mississippiensis, Crocodylus porosus, and Crocodylus novaeguineae were studied through gross dissection. Additionally, serial sectioned specimens of each of the above taxa, from the Ohio University Vertebrate Collections, were studied.

Several specimens were studied through the standard techniques of gross section. Most of these specimens were further studied, through the use of a hacksaw, as sagittal sections, a series of parasagittal sections, or a series of transverse sections. Other specimens were studied by removal of the mandible and/or removal of the skull roof.

Results

Proximal Branching and the Craniocervical Musculature

Common Carotid Artery and the Hypapophyseal Canal As in birds, the crocodilian common carotid artery travels rostrally, ventral to the

cervical vertebrae and dorsal to m. rectus capitis ventralis pars medialis whose muscle fibers

cross over the vessel before attaching to the vertebrae. Along each vertebrae, the dorsal

tendons of the right and left muscles travel rostrodorsomedially, across the dorsal aspect of

the common carotid artery and then insert on the ventrolateral aspect of a hypapophysis and

fuse with the tendon from the contralateral muscle. Each hypapophyseal aponeurosis is

connected to the hypapophyseal aponeurosis rostral and caudal to it by longitudinal

extension. This aponeurotic system ultimately forms a single longitudinal aponeurosis across the ventral cervical vertebrae that dorsally encloses the common carotid artery. As such, the carotid artery is enclosed laterally by fibers from the longus colli, ventrally by the dense muscle mass of the muscle body, and dorsally by the longitudinal hypapophyseal aponeurosis across the cervical vertebrae, thus forming an osseomuscular canal. Rathke (1866) illustrated 211 the carotid artery entering the cephalic region from a position dorsal to m. rectus capitis pars medialis.

The common carotid artery travels between the medial aspects of mm. rectus capitis ventralis pars medialis sinistra and dextra, and gives off a caudal branch toward the thyroid gland. The artery to the thyroid gland then sends off branches that ramify across, and partially supply a plexus within, the longitudinally elongate gland.

Ventral to the C1-C2 vertebral joint, the common carotid artery divides into left and right vessels, each of which turns laterally, crossing over m. rectus capitis ventralis pars lateralis, an oblique, ventrally directed muscle that attaches to the basal tubera on the rostroventrolateral aspect of the basioccipital, in a position ventral to the insertion of m. rectus capitis lateralis, and lateral to the insertion of m. rectus capitis dorsalis (Chiasson

1962). In this region, the common carotid artery lies deep to the jugular vein and some branches of the glossopharyngeal, vagal, and hypoglossal nerves. Medial to these structures is m. pterygoideus ventralis and the caudomedial aspect of the articular bone. The common carotid artery travels across m. recuts capitis ventralis pars medialis, and then curves dorsolaterally over the ventral and then the lateral aspects of the tendon of m. rectus capitis ventralis pars lateralis, and curves along the medial aspect of m. depressor mandibulae. The common carotid artery then bifurcates into dorsal and rostral branches, the external and internal carotid arteries, respectively (Owen 1850, termed the ecto- and enctocarotid arteries by the author; Reese 1914). Figure 10A-D depict the major cephalic arteries and their relationships to the bony skull. 212 External Carotid Artery The external carotid artery courses rostrodorsally across the lateral aspect of the m. rectus capitis dorsalis tendon and bifurcates into dorsal and ventral branches, the occipital and externostapedial trunks, respectively. The externostapedial trunk courses dorsolaterally across a robust rostrodorsolaterally oriented ridge along the exoccipital that forms the lateral aspect of the foramen magnum, and the medial border of fossa in the caudoventral surface of the bone that contains the vagus and hypoglossal foramina, and ventrolaterally, the external ostium of the internal carotid artery. The fossa in the exoccipital is analogous, if not homologous, to the parabasal fossa in birds. The ridge is rostrodorsolaterally confluent with the ventral aspect of the paroccipital process, which forms the dorsal border of the exoccipital fossa. The external carotid artery travels dorsolaterally toward the external ostium of the stapedial canal, along the ventral aspect of the ventral border of the paroccipital process, and across the rostral face of m. splenius capitis. The external ostium of the stapedial canal rests dorsolateral to the exoccipital fossa.

Occipital Artery The occipital artery courses dorsally, lateral to but not along, the dorsolateral aspect of m. rectus capitis dorsalis, and bifurcates into caudal and rostral branches, the superficial and deep occipital arteries, respectively. The superficial occipital artery travels caudodorsally across the lateral aspect of m. rectus capitis dorsalis, and then courses caudally between the ventrolateral aspect of m. biventer cervicis and the dorsomedial aspect of m. rectus capitis lateralis.

The deep occipital artery travels ventromedially to m. rectus capitis dorsalis and then sends off a caudal branch, m. rectus capitis lateralis artery, that courses caudoventrally to the rostromedial aspect of the fleshy m. rectus capitis lateralis. 213 The deep occipital artery travels dorsal to the dorsolateralmost aspect of m. rectus capitis dorsalis, and sends off a branch that travels dorsally across the atlanto-occipital joint capsule and that then passes medially through the first intervertebral foramen and enters the vertebral canal. The deep occipital artery then courses rostrally across the lateral aspect of the nerve to m. rectus lateralis, and then trifurcates into dorsal, rostroventral, and rostral branches.

The dorsal branch, the dorsal occipital artery, courses dorsally between the rostrolateral aspect of m. biventer cervicis and the rostromedial aspect of m. splenius capitis, and then travels to and then across the dorsolateral aspect of the former muscle to the rostroventral aspect of m. complexus. The vessel then courses caudally along the mid- ventral aspect of m. complexus and between the dorsolateral aspect of m. biventer cervicis and the dorsomedial aspect of m. splenius capitis (Rathke 1866; Hochstetter 1906), sending off vessels into each of them. The rostroventral branch of the trifurcation courses to the lateral aspect of the vagus nerve, and then travels caudoventrally along the nerve’s lateral aspect.

The rostral branch of the trifurcation courses toward the caudal aspect of the vagus nerve where the nerve exits the external vagus foramen. The vessel then travels across the medial aspect of a caudoventrally running cervical nerve, and then turns and courses ventrally across the medial aspect of the vagus nerve, then across the medial aspect of m. rectus capitis dorsalis, and then along the craniocervical joint capsule. The vessel then turns caudally, and courses caudally along the ventrolateral aspect of the vertebral column and the medial aspect of m. rectus capitis dorsalis. Dorsal branches of this last artery travel across 214 the lateral aspect of the cervical vertebrae, dorsal to the vertebrarterial canal, whereas ventral branches of the artery eventually travel through the vertebrarterial canal.

Proper External Carotid Artery A short distance further ventrolateral, the proper external carotid artery divides into the temporomandibular and oromandibular trunks at the dorsocaudomedial aspect of m. pterygoideus ventralis, near the muscle’s insertion into the internal mandibular process. The temporomandibular artery then travels rostrally across and then past the dorsomedialmost aspect of the m. pterygoideus ventralis tendon, and then continues to travel rostrally, across the ventral aspect of m. depressor mandibulae to the caudoventromedialmost aspect of the mandibular condyle of the quadrate.

Internal Carotid Artery The internal carotid artery travels rostrodorsally across the rostrolateralmost aspect of the tendon of m. rectus capitis ventralis pars lateralis. In its course toward the external ostium of the cranial carotid canal, the artery is laterally cross by the vagus nerve, and further rostrally by the glossopharyngeal nerve. Just rostral to the latter nerve, the artery gives off a medial branch that travels rostroventrally and eventually ramifies into a series of vessels within the thin tissue in the lateral pharyngeal wall, and that contribute to the supply of the richly vascular lateral pharyngeal diverticulum. The internal carotid artery then enters the external ostium of the osseous cranial carotid canal in a position just dorsal to the tendinous insertion of m. rectus capitis ventralis pars lateralis and dorsolateral to the tendon of m. rectus capitis dorsalis. The external ostium is located in the caudoventrolateral aspect of the exoccipital (Owen 1950), ventrolateral to the vagus foramen. 215 The vessel courses rostrodorsolaterally through the canal, situated in the ventrolateral otoccipital, and opens into the middle ear space through the internal ostium of the osseous cranial carotid canal. The internal ostium opens off the end of an osseous tube that extends from the otoccipital (Owen 1850). The protruding osseous tube opens medial to the ventral aspect of an oblique, ventromedial to rostrodorsally oriented ridge along the rostromedial aspect of the otoccipital. Caudal to this ridge and thus separated from the cranial carotid canal are the internal vestibulocochlear foramina, and dorsal to these foramina is a deep groove that parallels the above mentioned ridge. The latter groove is dorsolaterally confluent with the temporoorbital groove.

The protruding cranial carotid tube rests dorsal to the internal ostium (tympanic opening) for the pharygotympanic sinus, which in this area is confluent with the basioccipital sinus, which is formed by a caudodorsal diverticulum of the epithelium of Rathke’s pouch.

The medial wall of the rostral aspect of the cranial carotid canal within the otoccipital is the bony lateral border for an air space within the otoccipital that is confluent with, and formed by, the basioccipital sinus.

The cranial carotid canal is continued by a thick cartilaginous tube that courses through the middle ear space toward the internal carotid foramen, which is located in the lateral aspect of the basisphenoid. Owen (1850) described the vessel in this region of its pathway as covered by a “reflection of its living membrane.” Early in its course, the cartilaginous cranial carotid canal and the internal carotid artery and vein that travel through it travel rostroventrolaterally across the ventrolateral aspect of the opisthotic contribution to the otic capsule (Owen 1859; Shiino 1914), toward the caudodorsomedial aspect of the basiparasphenoid. In the rostral aspect of this course, the canal travels lateral to a rostral 216 foramen-like internal opening of the pharyngotympanic tube, and then turns rostromedially toward the rostral osseous component of the cranial carotid canal (Owen 1850). This rostral bony component of the canal is formed by a caudolaterally oriented groove in the caudodorsolateral basiparasphenoid, located rostral to the pharygotympanic ostium, and which has a low caudal ridge and a higher rostral ridge that form the side walls of the canal.

The higher rostral ridge completely separates the carotid canal from the more rostral and partly parallel facial nerve canal. The dorsal aspect of this aspect of the cranial carotid canal is unossified, but is covered by thick cartilage continuous with the cranial carotid tube.

The cranial carotid canal ends at the internal carotid foramen, and the vessels then course through a rostroventromedially oriented canal within the basisphenoid. It is unclear if the internal carotid artery sends off any “sphenoid vessels,” either a single sphenoid artery or separated sphenopalatine and sphenomaxillary arteries (see below). For this reason, it is unclear if the vessel entering the internal carotid canal should be termed the cerebral carotid or remain the internal carotid artery.

Further rostral in the basisphenoid, the canal runs more directly longitudinal and laterally parallels the canal of the abducens nerve as the latter runs through the basisphenoid.

The cranial carotid canal ends at a foramen that opens into the caudal hypophyseal fossa

(Owen 1850; Shiino 1914). After passing into the hypophyseal fossa, the internal carotid artery sends off a medial branch that travels medially and anastomoses with the contralateral branch, forming a horizontally oriented intercarotid anastomosis in the median caudal aspect of the canal. The configuration of the intercarotid anastomosis in crocodilians is H- shaped (Baumel and Gerchman 1968), and is similar in form to the intercarotid anastomosis of ratites. 217 Sphenoid Artery Upon reaching the dorsal component of the lateral aspect of the basisphenoid, the

palatine ramus of the facial nerve (CN VIIp) travels rostroventrally through a groove along the rostrolateral aspect of the basisphenoid. Ventrally the nerve and groove descend ventrally to a dorsally open foramen that leads into a canal. The canal runs rostroventrally and turns to run a short rostral distance through the ventrolateral aspect of the bony basisphenoid complex. The lateral aspect of this canal is formed by a groove that runs rostrally across the lateral aspect of the basisphenoid and across the dorsomedial aspect of the basipterygoid process. In at least one specimen of Alligator, an osseous tube encloses the rostral, lateral, and caudal aspects of the facial nerve in the nerve’s descent across the lateral aspect of the basisphenoid. This canal was dorsolaterally open, and two very small caliber arteries entered the tube through this opening, and then passed through the tube in a

position lateral to CN VIIp.

Caudally, the arteries that travel through the osseous tube run along the floor of the

dorsal aspect of the facial nerve canal to the opening in the middle ear space, lateral to the

caudal opening of the more rostral osseous cranial carotid canal. The floor of the proximal

CN VIIp canal is lined by a thick white connective tissue caudally continuous with the

rostroventral component of the cartilaginous cranial carotid artery tube, and the arteries

travel dorsal to the prootic periosteum and ventral to the connective tissue floor. It then

seems likely that these arteries branch from the cerebral carotid artery, but I produced no

specimens that demonstrated this connection.

The canal of CN VIIp and the sphenoid artery open into an area between the mid-

ventromedial aspect of the basisphenoid process of the pterygoid and the caudoventrolateral

surface of the parasphenoid rostrum through a foramen. This foramen is positioned 218 caudolateral to the caudoventral base of the parasphenoid rostrum and dorsomedial to the

basipterygoid process. CN VIIp and the sphenoid artery then course rostrally across the dorsomedial aspect of the pterygoid, the caudoventrolateral surface of the parasphenoid rostrum, and along the rostroventromedial surface of the basisphenoid process of the pterygoid (which is expanded rostrally in crocodilians beyond the basipterygoid process).

Further rostral, the sphenoid artery and CN VIIp enter into an area between the extreme ventromedial aspect of the orbit and the infraorbital space through a slit-like opening between the rostroventrolateralmost aspect of the parasphenoid rostrum and the rostroventromedialmost surface of the basisphenoid process of the pterygoid. This opening is positioned ventral to the tendinous insertion of m. retractor bulbi. Upon entering the orbital region, the sphenoid artery immediately anastomoses with a much larger vessel derived from the rostral ramus of the trigeminal artery.

Encephalic Vasculature of Extant Crocodylia

Major Osteological Correlates of Encephalic Vascular Structures Tentorial Crest

The origin of the tentorial crest is ventrally confluent with the lateral aspect of the dorsum sellae. The crest extends laterally from the dorsum sellae, then across the laterosphenoid-basisphenoid suture. The crest then extends dorsally along the caudal border of the laterosphenoid and proximally forms the rostral border of the trigeminal foramen.

The tentorial crest forms the caudal border of the rostral cranial fossa. The trochlear foramen is located in the caudoventrolateral aspect of the cerebral fossa, just rostroventral to the tentorial crest. Further dorsal, in a position rostral to the prootic-laterosphenoid-parietal sutural area, the crest becomes inflected slightly rostral and forms the rostroventral margin 219 of fossa tecti mesencephali. Rostrodorsally, the crest extends across the parietal-

laterosphenoid border, becomes medially inflected, and forms the rostrodorsal margin of the

fossa tecti mesencephali. This last aspect of the crest is termed the protuberantia tentorialis

(Elzanowski and Galton 1991). The protuberantia tentorialis and its extension, the marginal

crest, will be discussed further below.

Osteological Correlates of the Rostral Petrosal Sinus and External Occipital Vein

The rostral semicircular eminence (eminentia semicircularis rostralis) originates at the

caudoventral border of the supraoccipital bone, and more specifically originates from the

ventral area of the supraoccipital that forms the dorsal border of the endolymphatic duct

foramen. The eminence then travels along a dorsally inclined arch to the area where the

caudodorsomedial aspect of the bone, underlying the occipital pneumatic space, inflects

medially to form the supraoccipital shelf that roof’s the caudal endocranial cavity. At this

point the eminence arches and travels rostrodorsally, and then curves rostroventrally along

the mid-aspect of the supraoccipital before terminating at the prootic-supraoccipital suture.

The external occipital vein sulcus is rostrodorsal to the rostral semicircular eminence, and

the rostral aspect of the eminence sits within the endolymphatic fossa. It is important to

note that the rostral semicircular eminence is either faint or non-existent in adult Alligator

specimens, and is well pronounced in Crocodylus. However, the eminence is quite prominent

in hatchling specimens of Gavialis, Tomistoma, Crocodylus, Caiman, and Alligator. The eminence can be seen to become progressively less developed with age. Again, at these early stages, the eminence in Alligator is not as pronounced as in other crocodilians.

In juvenile alligators, the rostroventral aspect of the rostral semicircular canal

eminence extends to the rostrodorsal border of the trigeminal foramen and contacts the 220 tentorial crest, effectively eliminating the sulcus for the rostral petrosal sinus. In adult alligators the bone of the tentorial crest and the semicircular eminence is smoothly confluent and the eminence appears as a curved, caudodorsally oriented projection off the tentorial crest. Further caudodorsally, the rostral aspect of the rostral semicircular eminence forms the caudal border of the mesencephalic fossa and rostrally borders the cerebellum.

The sutural contact between the parietal, prootic, and laterosphenoid lies within the median portion of the mesenchephalic fossa, along the fossa’s vertical axis. Thus, the fossa is encompassed by the caudodorsalmost aspect of the laterosphenoid, the caudoventral aspect of the parietal, and is just rostral to rostrodorsal aspect of the prootic.

In crocodylids, the semicircular eminence does not extend as far ventral as the internal trigeminal foramen, and never contacts the tentorial crest. Rather, crocodylids

(especially juveniles) have a well defined sulcus for the rostral petrosal sinus that originates dorsal to the trigeminal foramen, and caudal to the tentorial crest, and that curves dorsocaudally around the rostral contour of the rostral semicircular eminence (originally grooving between the tentorial crest and the semicircular eminence). The caudal aspect of the sulcus for the rostral petrosal sinus is termed the sulcus for the rostral semicircular vein, a depression in the rostrodorsal surface of the epiotic, along the dorsal contour of the rostral semicircular eminence. The external occipital vein foramina (or single foramen) are located within the caudal aspect of the sulcus, and along the caudal aspect of the parietal-epiotic suture. A crest extends dorsally along the rostralmost aspect of the epiotic, rostral to the external occipital vein foramen, and forms the caudal border of the mesencephalic fossa 221 An apparent expansion of the rostral semicircular eminence in Alligator seems to have cut off the venous flow dorsal to the trigeminal foramen and thus eliminated the rostral semicircular vein. Neither adult nor juvenile alligators have an external occipital foramen.

Cerebellar Auricular Fossa and Sinus

In hatchling crocodilians, the rostral semicircular eminence serves as a bony border

for a large component of the cerebellar auricular fossa (or floccular recess). The crocodilian

recess is never as deep as in the cerebellar auricular fossa of birds. The cerebellar auricular

fossa is formed by and contains the cerebellar auricle, which is well developed in hatchling

crocodilians. The fossa is obliquely oriented with a caudodorsal to rostroventral orientation.

The caudodorsal aspect of the fossa is formed by a recess in the endocranial rostroventral

aspect of the epiotic, and the fossa extends rostroventrally as a recess in the caudodorsal

aspect of the prootic. The fossa is bordered caudodorsally by the rostral face of the caudal

aspect of the rostral semicircular eminence, dorsally by the ventral face of the dorsal aspect

of the eminence, and rostrally by the caudal face of the rostral aspect of the eminence. The

ventral aspect of the fossa is bordered by the rostrodorsal aspect of the otic capsule. In

several Alligator specimens a single larger foramen is located in the caudodorsalmost aspect

of the fossa, as in birds. In adult Alligator specimens, the rostral semicircular eminence is no

longer detectable and the cerebellar auricular fossa is much shallower. A smaller number of

Alligator and Crocodylus specimens featured a scattering off small foramina in the epiotic in

the caudodorsalmost aspect of the cerebellar auricular fossa rather than a single foramen. In

Alligator, the auricular vein draining from/into the auricular foramen travels rostroventrally

across the caudodorsal aspect of the cerebellar auricular fossa, to and then across the caudal

face of the rostral aspect of the rostral semicircular eminence. The vein then travels 222 rostrocaudally for a short distance across the caudal aspect of the laterosphenoid crest and empties into (or branches from) the trigeminal vein.

The cerebellar fossa (fossa cerebelli) is formed by and contains the lateral aspects of the cerebellum. The depression is found within the middle aspect of the dorsal prootic, dorsal to the medial trigeminal foramen, and more caudally sits within the rostroventral

(prootic) face of the otic capsule. In adult alligators, the deepest section of the fossa lies rostral to the otic capsule and likely represents a shallow remnant of the cerebellar auricular fossa. Rostrodorsally, the fossa is bordered by the caudal aspect of the marginal crest. The cerebellar fossa is caudodorsally confluent with a depression in the epiotic dorsal to the epiotic-prootic suture that contains the endolymphatic duct.

Metotic Fissure

The metotic fissure is bordered rostroventrally by the prootic, ventrally by the basisphenoid-basioccipital sutural area, rostrodorsally by the rostrolateral wing of the opisthotic, and caudally by the caudal ridge of the accessory nerve fossa in the exoccipital

(see below).

Encephalic Arterial System At the caudal aspect of the hypophyseal fossa, the cerebral carotid bifurcates into rostral and dorsal branches, the orbital and common encephalic arteries, respectively. See

Figure 11 for a depiction of the encephalic arteries within the braincase. The common encephalic artery immediately gives off anastomosing rostral branches to the hypophysis that communicate with the contralateral hypophysis vessels via an anastomotic vessel that extends across the hypophyseal floor. The common encephalic artery continues dorsally along the medial aspect of the lateral wall of the sella turcica. Along the dorsolateral aspect 223 of the dorsum sellae, the artery divides into dorsal and caudal branches, the rostral and caudal encephalic arteries, respectively.

The rostral encephalic artery courses dorsally and divides along the floor of the rostral cranial fossa into rostral and dorsal branches. The rostral branch passes along the floor of the cerebral fossa against the lateral aspect of the laterosphenoid wall, and gives off small ventral vessels that anastomose in the plexus supplying the hypophysis. The vessel then divides into the middle and rostral cerebral arteries.

The middle cerebral artery has a torturous course, arching caudally and then rostrodorsally on the lateral side of the cerebrum (Shiino 1914). Along its course, the middle cerebral artery gives off dorsomedial arteries into the cerebrum. The middle cerebral artery terminates through anastomotic vessels with the rostral cerebral and interhemispheric arteries.

The rostral cerebral artery passes across the ventromedial aspect of the laterosphenoid, ventral to the cerebral fossa, and on the rostroventral surface of the cerebrum (Shiino 1914). The artery first gives of a number of small caliber vessels ventromedially into the plexus surrounding the hypophysis. The artery continues rostrally and divides, midway in its course, into a large dorsal branch and a smaller rostral branch.

The dorsal branch travels tortuously up the midline of the cerebral fossa of the laterosphenoid on the surface of the rostral cerebrum. This dorsal branch then turns rostrodorsally to follow the contours of the cerebrum until reaching the dorsal aspect of the cerebrum, after which the vessels continue across the rostrodorsal cerebral surface before anastomosing with the interhemispheric artery. The rostral branch follows along the surface of the rostroventral cerebrum (Shiino 1914), becomes medially inclined away from the 224 rostroventral border of the laterosphenoid, and sends off a number of closely bunched arteries that parallel its course and spread across the cerebrum. At its terminus, the rostral cerebral becomes dorsomedially inclined and anastomoses with the contralateral rostral cerebral artery to form a single vessel (Craige 1941) that travels rostrally across the rostroventralmost surface of the cerebrum, and then courses rostrally along the ventral aspect of the olfactory tract (Shiino 1914).

The dorsal branch off the rostral encephalic artery, the caudal cerebral artery, travels along a curved dorsal path in a position just rostral to the tentorial crest. Rostral to the rostroventral aspect of the mesencephalic fossa, the vessel abruptly curves medially and gives off several small vessels to the ventral, caudal, and rostral aspects of the cerebrum. The vessel continues along the caudolateral aspect of the cerebrum where it nearly touches the contralateral caudal cerebral artery. The two arteries curve dorsally together along the caudal aspect of, and send rostral vessels into, the cerebrum. The vessels then take a tortuous S- shaped course, first turning away from one another in a sharp lateral direction and sending off vessels to the mesencephalon. The continuations of the two caudal cerebral arteries, the interhemispheric arteries, then curve again medially towards one another and meet in the midline on the caudodorsal surface of the cerebrum, after which the two arteries closely parallel each other in a rostral course across the interhemispheric fissure of the cerebrum, sending ventrally directed vessels into the two cerebral hemispheres. Along the rostral dorsal cerebral surface, the caudal cerebral arteries give off vessels that anastomose with branches of the rostral and middle cerebral arteries. At the rostralmost aspect of the cerebrum, the caudal cerebral arteries anastomose with one another to form a single common olfactory artery that runs rostrally across the dorsal surface of the olfactory tract. 225 According to Craige (1941), in most crocodilians and birds, the caudal cerebral artery

arises from the rostral encephalic artery (along with the rostral and middle cerebral arteries),

whereas in Alligator mississippiensis the caudal cerebral artery arises from the caudal encephalic artery (as in mammals and turtles). The caudal cerebral artery was a branch of the rostral encephalic artery in most of the Alligator specimens observed in this study.

The caudal encephalic artery arches caudodorsally across the caudal border of the

hypophyseal fossa, then onto the dorsal surface of the dorsum sellae, and then divides into

dorsal and caudal branches. The dorsal branch runs on the medial aspect of the dorsal

continuance of the dorsum sellae that develops into the tentorial crest. The vessel continues

in a dorsal direction, eventually running along the medial aspect of the tentorial crest and

rostral to the mesencephalic fossa where it breaks up into a dense array of vessels that supply

the mesencephalon. The vessels sends off rostromedially directed vessels into the

mesencephalon and several large vessels that turn caudally and then medially to supply the

caudal aspect of the mesencephalon and the rostral cerebellum.

The caudal branch of the caudal encephalic artery arches over the dorsum sellae and

travels caudomedially across the caudal aspect of the dorsum sellae and sends off a vessel

that travels caudoventrolaterally across the caudal slope of the dorsum sellae toward the

rostromedial aspect of the internal trigeminal foramen. The caudal branch of the caudal

encephalic artery then continues caudomedially across the dorsum sellae and unites with the

contralateral vessel to form a single basilar artery. On the caudoventral aspect of the dorsum

sellae, the basilar artery sends off a lateral branch that curves dorsally, rostral to the

trigeminal foramen and caudal to the marginal crest, then curves caudodorsally across the 226 dorsal surface of the maxillomandibular ganglion and gives off rostral and medial branches to the ventral aspect of the mesencephalon.

The first large branch of the basilar artery travels laterally across the median dorsal aspect of the basisphenoid toward the medial aspect of the internal trigeminal foramen and turns to course rostrolaterally toward the foramen. The artery ultimately anastomoses with the artery off the caudal branch of the caudal encephalic artery discussed above, and forms the trigeminal artery, ventral to the maxillomandibular ganglion. The vessel then travels laterally across the floor of the canal and bifurcates into caudal and rostral branches. The rostral branch travels with the profundus nerve through the profundus canal, whereas the caudal branch travels laterally through the maxillomandibular canal.

Just rostral to the basioccipital-basisphenoid juncture, the basilar artery sends off a large caliber vessel, the caudoventral cerebellar artery, that runs laterally across the caudodorsal surface of the basisphenoid and then splits rostrally and caudally around the metotic fissure, between the prootic and the opisthotic. The artery travels dorsally along the prootic to the ventral aspect of the prootic portion of the otic capsule and then divides into a rostral branch that anastomoses over the trigeminal nerve with vessels from the dorsal cerebellar artery, and a caudal branch that travels caudodorsally across the otic capsule and along the rostroventral surface of the cerebellum. The caudal branch passes caudolaterally, ventral to the metotic fissure and then divides into rostral and caudal branches. The rostral branch curves caudal to the metotic fissure and the glossopharyngeal nerve and dorsal to the ventral aspect of the otic capsule where it ramifies across the prootic contribution to the otic capsule and along the caudoventral aspect of the cerebellum. The caudal vessel travels in a 227 tortuous caudolateral direction ventral to the otic capsule in a series of loops, and gives off a long dorsal vessel across the rostromedial surface of the opisthotic.

Caudal to the basisphenoid, the basilar artery becomes tortuous in its course across the basioccipital and spits into a branch that follows a caudodorsal course across the medulla and a small ventral branch, the spinal artery, that continues along the braincase floor and through the foramen magnum to run ventral to the spinal cord.

Encephalic Venous Sinuses

Ventral and Dorsal Sagittal Sinuses

The falx cerebri cleaves between the cerebral hemispheres, and the dorsal sagittal sinus runs through the dorsalmost aspect of the falx cerebri, and the ventral sagittal sinus runs through the ventral aspect of the falx cerebri, receiving veins that drain the ventral cerebrum. Toward the caudal median aspect of the cerebral hemispheres and rostral to the paraphysis, the ventral sagittal sinus begins to curve caudodorsally along the falx cerebri.

The ventral sagittal sinus travels along the caudodorsalmost aspect of the falx cerebri and then drains into the dorsal sagittal sinus. Veins associated with the rostroventral and ventrolateral components of the epiphysis body travel rostrally between the cerebral meningeal sheaths and drain into the ventral sagittal sinus as the latter vessel begins its course toward the dorsal sagittal sinus. The vessel that (1) results from the drainage of veins from the ventral cerebrum, the paraphysis, and aspects of the diencephalon and mesencephalon into the ventral sagittal sinus, and that (2) subsequently anastomoses with the dorsal sagittal sinus can be considered analogous, or potentially homologous to, the mammalian straight sinus. 228 The dorsal sagittal sinus is the endocranial continuation of the olfactory sinus, and

travels caudally across the median aspect of the endocranial surface of the frontal. The

dorsal sagittal sinus travels along the dorsal aspect of the interhemispheric arteries.

Sphenotemporal Sinus

The caudolateral component of the cerebrum rests, in part, against the rostral face of the tentorial crest. The dura associated with or originating from the tentorial crest and laterosphenoid ridge protrudes medially and forms a thick wedge between the caudal cerebrum and the rostral mesencephalon. In a parasagittal section the dural wedge appears triangular with the apex oriented ventrally, and the entire dural structure appears hollow. The sphenotemporal sinus courses between, and drains, the caudodorsal cerebrum and rostrodorsal mesencephalon, and is contained within the dural sleeve that protrudes between the two neural regions. In corrosion casts and specimens that were dissected after latex injection, this vessel appears as a small size sinus. However, the small size of the sinus in the prepared specimens may be an artifact of filling during injection, and it is entirely possible that venous blood filled the entire triangular, hollow space between the meningeal sleeves that cleave between the mesencephalon and cerebrum. The sinus does receive a series of veins that drain from the caudalmost cerebrum and from the lateral aspects of the more caudal half of the cerebrum, and further drains the rostral face and lateral aspect of the mesencephalon. The sinus travels dorsally and slightly caudally across the rostromedial aspect of the tentorial crest and then with the crest across the laterosphenoid-parietal suture, and then courses caudomedially across the ventral surface of the protuberantia tentorialis and is now termed the transverse sinus. 229 Torcular Herophili

The protuberantia tentorialis turns medially and extends across the parietal and

becomes confluent with the contralateral marginal crest to form a wide and robust

horizontal ridge, the marginal crest that forms the caudodorsal border of the rostral cranial

fossa and the rostrodorsal border of the middle cranial fossa. A large, deep, oval fossa is

located in the center of the endocranial aspect of the parietal and extends across the rostral

face of the marginal crest, which demarcates the caudal and caudolateral borders of the

parietal fossa. The fossa contains and is likely formed by a huge central venous sinus, the

torcular herophili (Wharton 2000). The dorsal sagittal sinus empties into the mid-

rostralmost aspect of the torcular herophili sinus (Hopson 1979). The transverse sinus

travels across the ventral aspect of the marginal crest and near the crest’s median surface, the

sinus drains into the torcular herophili (Hopson 1979). Additionally, the single, large “great

cerebral” vein travels along the tissue of the paraphysis in the organ’s dorsal course toward the ventral parietal fossa, and drains into the center of the torcular herophili. Thus, the torcular herophili is formed by the confluence between the dorsal sagittal, transverse, and ventral sagittal sinuses and the “great cerebral” vein and its tributaries. In most injected specimens, the sphenotemporal sinus is first evidenced along the mid aspect of the rostral laterosphenoid ridge near the origin of the tentorial crest, and it is unclear that the vessel continues ventrally toward and anastomoses with the cavernous sinus.

At the rostrodorsalmost aspect of the marginal crest, the mid-ventral aspect of the

caudal apex of the torcular herophili constricts and is caudally continued by a single median

venous sinus, larger in size than the dorsal sagittal sinus, and termed the occipital sinus

(Hopson 1979). This venous sinus courses caudoventrally across the rostral face of the 230 marginal crest, and then curves caudally across the ventral aspect of the marginal crest, and

courses across the caudoventralmost aspect of the parietal. Finally, the sinus courses

caudodorsally along the caudal face of the rostral border of the occipital sinus fossa and

drains into the confluences of sinuses near the sutural contact between the parietal and

rostroventralmost aspect of the supraoccipital.

Rostral Petrosal Sinus

Formation of the Rostral Petrosal Sinus The caudoventral cerebral vein originates from the dorsal division of a sinus extending across the dorsum sellae, and drains laterally across the caudodorsolateral aspect of the dorsum sellae. The vessel then drains caudodorsally across the caudomedial face of crest, the caudoventral aspect of the cerebrum, and the rostral aspect of the maxillomandibular trigeminal ganglion in its passage into the internal trigeminal foramen.

The vein then travels along the caudoventral aspect of the tentorial crest and the dorsal aspect of the maxillomandibular trigeminal ganglion and the internal trigeminal foramen.

Another vein, the rostroventral cerebellar vein travels dorsally and rostrally around, and drains, the caudal aspect of the maxillomandibular trigeminal ganglion. Further dorsal, the vein courses along the rostroventrolateral aspect of the cerebellum. A series of tributaries course from the cerebellum and then drain into the vein. In its course, the rostral cerebellar vein travels along the rostroventral surface of the prootic and the caudal border of the internal trigeminal foramen, and finally arrives at an area dorsal to the trigeminal foramen, at which point the vein anastomoses with the caudoventral cerebral vein and receives veins that drain from the trigeminal canal and forms the rostral petrosal sinus. 231 Internal Trigeminal Foramen The internal trigeminal foramen is covered by a thick, white connective tissue, which appears to be continuous with the endocranium and/or the dura. This trigeminal covering is perforated in several area by nerve fibers, which greatly complicated the anatomy of the structure. It is also possible that the pattern of perforation is variable. It is important to note that the medial trigeminal foramen in crocodilians is obliquely oriented along an axis with the rostral aspect being more ventrally inclined and the caudal aspect more dorsally inclined. As an example, in a specimen of Alligator mississippiensis there is a large opening between the laterosphenoid bone and the tissue wall in the rostroventralmost aspect of the trigeminal foramen, in which two large nerves pass through, most likely derived from the profundus nerve. The caudodorsal aspect of the foramen is divided in midsection by a thick strip of the tissue wall, and on either side of this strip is a large opening between the tissue and the prootic bone. Through each of these dorsal foramina pass a large nerve and a vein or venous network that drains into the anastomotic vein dorsal to the medial trigeminal foramen, which then drains into the transverse sinus. Between the more rostral of these dorsal openings and the rostroventral opening are a further three large opening between the tissue wall and the laterosphenoid. Ventral to the more caudal of the dorsal openings along the mid aspect of the caudal component of the trigeminal foramen is a single large opening between the prootic and the tissue wall for a single large nerve. The center of the tissue wall is a series of three paired, vertically oriented rows of smaller openings, each of which is perforated by a smaller nerve.

Course of the Rostral Petrosal Sinus In Alligator, the rostral petrosal sinus is an enormous venous sinus that spreads across the width of the rostroventral aspect of the rostral semicircular eminence. The sinus 232 protrudes medially and cleaves between the caudal aspect of the optic tectum and the rostral aspect of the cerebellum, draining the caudal and rostral aspect of these two structures, respectively. The sinus drains caudodorsally across the rostrodorsomedial aspect of the prootic, and across the rostral curvature of the cerebellum. Caudodorsally, the sinus travels across the cerebellar fossa that extends across the rostrodorsal aspect of the otic capsule, just caudal to the parietal-supraoccipital suture. Further caudodorsally the sinus travels through the fossa as it extends just caudal to the rostroventromedial parietal-supraoccipital suture, which marks the dorsolateral border of the endocranial wall. From here, the sinus drains caudodorsally across the dorsomedial aspect of the otic capsule, and then travels caudodorsomedially to and across the endocranial roof. Throughout its path, the sinus travels just caudal to the parietal-supraoccipital suture. The sinus eventually drains into the occipital sinus (Hopson 1979) near the median aspect of the endocranial roof caudal to the parietal-supraoccipital suture. In birds, the aspect of the rostral petrosal sinus that drains into the occipital sinus is termed the caudal petrosal sinus (see Chapter 2). Additionally, the aspect of the rostral petrosal sinus that courses across the dorsal aspect of the rostral semicircular eminence is termed the rostral semicircular vein in birds.

As mentioned above, crocodylids retain the ancestral archosaurian system of grooves associated with the course of the rostral petrosal sinus, and the course of the sinus would follow the path of the groove outlined above (see Figure 11).

Caudal to the intersection of the two rostral petrosal sinuses and the occipital, this confluence of sinuses expands to form a somewhat circular venous sinus that fills a large fossa in the center of the rostroventral aspect of the supraoccipital. The endolymphatic sac rests in this area, in the epiotic, dorsal to the dorsal aspect of the cerebellum, along the lateral 233 aspect of the endocranial roof, and just caudal to the caudomedially oriented aspect of the

rostral semicircular eminence. When filled with endolymph, the sac bulges medially, and

constricts the occipital sinus by pushing the lateral aspect of the sinus medially. In this area,

the occipital sinus rests against the median dorsal aspect of the cerebellum.

Once released from the endolymphatic sac’s encroachment, the sinus expands to fill

the fossa of the occipital sinus, which comprises the entire roof of the endocranium caudal

to the sac. The rostral aspect of the fossa is formed by the caudoventralmost aspect of the

supraoccipital and the endocranial rostrodorsalmost aspect of the otoccipital. This bony

area of the rostral fossa is formed by a large, deep, caudoventrally oriented slope that is

strongly angled away from the longitudinally oriented and more rostroventral aspect of the

supraoccipital.

External Occipital Vein As mentioned above, in crocodylids there is a longitudinally oriented sulcus

containing a foramen (or foramina) along the rostrodorsal aspect of the supraoccipital just

caudal to the parietal and rostrodorsal to the rostral semicircular canal eminence. The

sulcus contains venous structures traveling from the rostral petrosal sinus that have branches

that pass through the small foramina and enter into the pneumatic space within the

supraoccipital and ramify to supply the tympanic sinus within this cavity. In juvenile

crocodylids, there is often a large foramen in this area that rests with the groove for the

rostral petrosal sinus. Again, the presence of a sulcus or foramina could not be identified in

any Alligator specimen.

Cavernous Sinus

A large circular sinus surrounds the hypophysis and the walls of the hypophyseal fossa. At the caudoventral aspect of the fossa, the sinus sends off the internal carotid veins 234 that travel caudally through the internal carotid canal with the internal carotid artery. The orbital vein courses through the optic foramen and drains into the rostrolateral aspect of the cavernous sinus.

At the midline of the rostroventral face of the caudal border of the hypopophyeal fossa, the cavernous sinus forms a single small caliber venous sinus that then courses dorsally across the border and to the rostrodorsal aspect of the dorsum sellae. On the dorsal aspect of the dorsum sella, the sinus sends off a large sinus from its lateral aspects which then courses laterally across the dorsum sellae. At the dorsolateral aspect of the dorsum sellae, the sinus divides into a dorsal and a ventral branch. The dorsal branch courses dorsally and drains into the caudoventral cerebral vein, situated along the lateral aspect of the tentorial crest. The ventral branch courses ventromedially across the caudal face of the dorsum sellae, and to the area of the basisphenoid caudal to the dorsum sellae. At this point, the sinus anastomoses with a vessel that travels rostroventrally from the aspect of the trigeminal sinus that rests ventral to the trigeminal foramen. The sinus then continues its caudomedial course and approaches the abducens foramen, after which the sinus splits and courses caudally around the lateral and medial aspects of the foramen, and then anastomoses with the abducens vein, just caudal to the latter vessel’s entrance into the endocranium.

Spinal Accessory Nerve

A large triangular swelling (the apex directed caudally) of the accessory nerve rests along the caudoventromedial aspect of the exoccipital, just medial to caudal aspect of the large, caudal, hypoglossal foramen. The apex of the swelling is continued by the spinal division of the nerve, which courses caudally, past the craniocervical joint, and then across 235 the medial face of the lateral aspect of the vertebral canal. The ventromedial aspect of the

swelling is derived from the cranial division of the nerve, which extends from the

caudoventrolateral aspect of the medulla. At the rostral aspect of the swelling, the nerve

splits into dorsal and ventral branches, that travel a steep rostrodorsal and rostroventral path,

respectively. The rostral component of the caudal hypoglossal nerve is exposed within its

foramen, just rostral to the bifurcation. The caudal hypoglossal nerve originates from the

medulla caudal to the accessory nerve’s bifurcation, and then travels rostrodorsally, across

the dorsolateral aspect of the ventral ramus of the accessory nerve, and enters the caudal

hypoglossal foramen caudally, lateral to the swelling, and then into the foramen.

The caudodorsal aspect of the ventral ramus of the accessory nerve rests between the roots

of the caudal and middle hypoglossal nerves. The ventral branch then courses

rostroventrally across the ventromedial aspect of the exoccipital and then becomes more

rostrally oriented, and travels rostroventrally across, and grooves, the mid-lateral aspect of

the accessory process. At the caudodorsal aspect of the process, the ventral ramus passes

through the pericranium, and subsequently travels external to this tissue. The accessory

process is a large, rugose, protuberance extending from the mid-dorsomedial aspect of the

basioccipital, and then across the medial basioccipital-exoccipital suture, and continues to protrude from the mid-ventromedialmost aspect of the exoccipital. The accessory nerve travels across, and grooves, the process along the basioccipital-exoccipital sutural contact.

After passing the rostral aspect of the process, the nerve continues its rostral path across the suture and then terminates after sending ventrally oriented nerves through small foramina and slits between the basioccipital and exoccipital. 236 The area of the medial exoccipital, caudal to the vagal fenestra, is characterized by a thick, caudally concave, semicircular ridge. The ventral component of the ridge stretches caudoventrally across the exoccipital toward the caudal two hypoglossal foramina, and then extends to the bony pillar separating the foramina, and terminates along the rostral aspect of the more rostral foramen (the middle hypoglossal foramen). The dorsal component of the ridge extends caudodorsally across the dorsomedial exoccipital toward the endocranial roof

(formed by a shelf protruding medially from the dorsomedial aspect of the exoccipital), and courses caudomedially across the roof toward the dorsal aspect of the foramen magnum.

This caudodorsal ridge marks the rostral border of the rostral aspects of the medulla’s caudodorsal extension. Moreover, the medulla inserts into the endocranial roof just caudal to the caudal aspect of the ridge as it protrudes from the roof.

The dorsal branch, which originates from the swelling caudodorsal to the caudal hypoglossal foramen, courses rostrodorsally across the rostral otoccipital, and the lateral aspect of the medulla. The nerve ends in the accessory nerve fossa, which is rostrally bordered by the caudal face of the central and rostralmost aspects of the semilunar ridge.

The fossa contains numerous small rostrally directed foramina into which the rostral aspect of the accessory nerve sends several small branches that then pass into the dorsal aspects of the vagal canal. The caudoventrolateral aspect of the opisthotic contribution to the otic capsule is just caudodorsal to the glossopharyngeal foramen, and expands caudomedially before turning into a rostroventrally inclined bony pillar that divides the vagal and glossopharyngeal foramina. The caudolateral expansion comprises the rostroventral aspect of the vagal vein groove, and within this aspect of this groove are a series of variably sized foramina, with openings that face caudomedially, or ventrally toward the internal vagus 237 foramen. However, as mentioned above, the venous groove continues to course within the vagal canal along the rostroventromedial aspect of the opisthotic contribution to the otic capsule. Within this latter groove, a series of foramina open rostroventrally into the internal glossopharyngeal foramen. Branches of the accessory nerve pass out of these foramina and then join with either the glossopharyngeal or vagus nerves.

The ventral aspect of the occipital sinus rests against the length of the dorsal ramus of the accessory nerve, and further caudoventrally, within the endocranial space, rests against the length of the dorsal aspect of the spinal division of the accessory nerve. Thus, the accessory nerve defines the ventral boundary of the occipital sinus.

Roots from the spinal cord travel rostrolaterally from the cord and joint the medial aspect of the spinal division of the accessory nerve. As in birds, the spinal division of the accessory nerve rests against the lateral aspect of the spinal cord, and between the dorsal and ventral roots of the spinal nerves. The branches of the spinal division, however, travel ventrolaterally, and exit the vertebral canal with the ventral roots.

Endolymphatic Sac

The caudolateral border of the endolymphatic sac attaches along the obliquely oriented (caudodorsal to rostroventral), epiotic-otoccipital sutural contact of the otic capsule.

The rostral border of the sac inserts along the epiotic ridge. The medial aspect of the epiotic is divided into caudal and rostral components by a vertically oriented ridge that begins just dorsal to the caudalmost aspect of the epiotic-prootic suture, just rostrodorsal to the endolymphatic foramen, and extends dorsally across the medial face of the epiotic to the epiotic contribution to the dorsolateral border of the bony endocranium. The ridge serves as the attachment of the rostrolateral aspect of the endolymphatic duct. The 238 endolymphatic foramen is situated at the intersection of the epiotic-otoccipital and epiotic-

prootic sutures, and is enclosed within the ventralmost aspect of the sac, which inserts

around the ventral border of the foramen. The epiotic-parietal suture caudal to the epiotic

ridge marks the rostrolateral border and insertion area of the sac.

Vagal Sinus

Just after passing the caudal endolymphatic sac, the occipital sinus gives off a lateral branch that courses caudoventrally through a groove situated between the caudolateral aspect of the opisthotic contribution to the otic capsule, and the rostrodorsomedial aspect of the exoccipital. In its dorsal course, the branch travels across the caudoventrolateral border of the endolymphatic sac. Upon entering the caudodorsolateral aspect of the vagal fenestra, the vein curves within the groove along the caudoventrolateral aspect of the opisthotic contribution to the otic capsule. This component of the opisthotic continues as a rostroventrally oriented bony pillar that divides the glossopharyngeal and vagal foramina.

The groove of the vagal vein courses to the caudodorsal border of the internal vagal glossopharyngeal foramen, and rests rostral to the vagal foramen. From here, the vein sends off a branch that passes into the internal vagal foramen, and rostrolaterally through the vagal canal, dorsal to the vagus nerve. Around the foramen and within the canal, this sinus-like vein forms a venous plexus that surrounds the nerve. The venous groove, continues to course within the vagal canal against the rostroventrolateral aspect of the opisthotic contribution to the otic capsule, across the rostral face of the exoccipital, and along the dorsal aspect of the glossopharyngeal foramen. The rostrolateral continuation of the vagal vein travels with the glossopharyngeal nerve through the glossopharyngeal canal, and like the 239 vagus vein, forms a plexus that surrounds the nerve. The entirety of the groove of the vagal sinus runs along the rostral aspects of the exoccipital.

Basilar Sinus

Through each abducens foramen, a large vein enters into the endocranial cavity from the orbit. As mentioned above, the abducens vein anastomoses with a caudoventrally oriented sinus originating from both the sinus of the dorsum sellae and the rostral petrosal sinus. The resulting large sinus, the basilar sinus, then courses caudoventrally across the lateral aspect of the basisphenoid and the ventrolateral aspect of the medulla. In its course, the sinus sends off vessels across the medial aspect of the basioccipital which anastomose with medial branches of the basilar sinus from the opposite side, and together these branches form a loosely connected plexus across the ventral aspect of the medulla. As the basisphenoid is angled ventrally from the caudal aspect of the dorsum sellae, and the basioccipital has an ever sharper ventral angulation, the basilar sinuses travel across the basioccipital in a steep caudoventral course. After passing across the basioccipital- basisphenoid suture, the two basilar sinuses become larger in size and send off medial branches that anastomose into a denser plexus across the dorsal basioccipital and the ventral medulla. Additionally, the basilar sinuses send off lateral branches that form an anastomotic plexus across the dorsolateral basioccipital. Further caudally, the basioccipital is characterized by a deep centrally located, longitudinally oriented fossa. In this area, the basilar sinus sends off medial branches that anastomose to form a particularly dense plexus spread throughout the dorsal basioccipital fossa.

Caudal to the basioccipital, the basilar sinus courses caudodorsally around the ventral aspect of the accessory process, and caudal to the process, the sinus travels along the 240 now caudodorsally oriented caudal aspect of the medulla. Near the rostralmost aspect of the basioccipital, caudal to the craniocervical joint, the two basilar sinuses travel caudomedially toward each other and then anastomose along the central caudal basioccipital in an area parallel to the position of the caudal hypoglossal foramen. The resulting sinus of the anastomosis then bifurcates into two sinuses, the caudal basilar sinuses, that course caudolaterally away from the sinus intersection, and subsequently travel caudally across the craniocervical joint. The arrangement of the inter-basilar sinus and the sinuses that contribute to and branch from it takes the form of an X. Another large sinus branches from the caudoventrolateral aspect of the occipital sinus and travels ventrally across the medial aspect of the exoccipital, the rostral aspect of the dorsal branch of the accessory nerve and the accessory nerve swelling, and the lateral aspect of the medulla. The ventral occipital sinus then passes across the rostral aspect of the caudal hypoglossal foramen, then courses across the lateral aspect of the ventral ramus of the accessory nerve, travels across the exoccipital-basioccipital suture, and then travels ventromedially across the ventrolateral medulla to drain into the lateral aspect of the caudal basilar sinus. The ventral aspects of the ventral occipital sinus become longitudinally wide and break up into a plexus that spreads across the lateral medulla and the ventromedial exoccipital. Aspects of the plexus cross to the basioccipital, and anastomose with the inter-basilar anastomoses and with the caudal basilar sinus. As a result of these last anastomoses, a single, enormous, venous sinus completely encircles the caudal aspects of the medulla, and spreads around the bony endocranium, in the area rostral to the craniocervical joint. 241 Metotic Sinus

Another sinus, the metotic sinus, courses into the endocranium, passing through the

metotic fenestra. Before entering the endocranium, the metotic sinus spans across the

entire length of the caudal aspect of the metotic fenestra. The more dorsal components of

this sinus anastomose into the vagal sinus near its entrance into the metotic fenestra.

Overall, the sinus tends to flow ventrally, and the largest area of the sinus is along the

caudoventral and ventral aspects of the metotic fenestra. The sinus then courses

caudoventromedially toward the basioccipital, crosses the exoccipital-basioccipital suture, then courses across the dorsolateralmost aspect of the basioccipital, and ends by draining

into the basilar sinus just before the latter vessel drains into the inter-basilar sinus.

Brief Survey of Cephalic Venous Drainage The dorsal aspect of the foramen magnum sinus extends caudally across the roof of

the craniovertebral joint and into the intravertebral canal, and then courses caudally across

the roof of the canal and the dorsal aspect of the spinal cord as the intravertebral venous

sinus (Hopson 1979).

A large venous plexus drains into a large vein that travels caudally from the ostium of

the median pharyngeal canal and travels across the median basioccipital crest and the dorsal

surface of m. rectus capitis ventralis pars medialis. At the caudal aspect of the crest the vein

divides into right and left branches that travel dorsolaterally across the ventral basioccipital

fossa that is located between the occipital condyle and the median basioccipital crest. The

vein then travels to the ventrolateral aspect of the occipital condyle and receives the internal

carotid vein, and then travels caudally across the ventrolateral surface of the cervical

vertebrae, and the dorsal surface of m. rectus capitis ventralis pars lateralis. Upon leaving 242 the cranial carotid canal, the internal carotid vein courses ventromedially across the exoccipital, lateral to the occipital condyle before the above anastomosis.

The lateral aspect of the foramen magnum sinus, as it becomes the intravertebral venous plexus, sends off a large vein that courses laterally (Hopson 1979) through the space between the exoccipital and the atlas vertebral apparatus. The vein then courses across the ventral aspect of the paroccipital process in a position ventral to the external carotid artery toward the external ostium of the stapedial canal. In birds, this vein would receive the external occipital vein and form the common occipital vein, that would then travel to the parabasal fossa. However, crocodilians lack an external occipital vein, so a true “common occipital vein” is not formed. The stapedial vein courses ventrally from the stapedial canal, across the paroccipital process, and drains into the lateral branch of the foramen magnum sinus, and forms the equivalent of the avian caudal cephalic vein. At this point, the temporomandibular vein drains into the lateral aspect of the caudal cephalic vein and forms the jugular vein. The jugular vein travels caudoventrally to the ventrolateral aspect of m. rectus capitis lateralis, and then travels caudally across the ventrolateral aspect of m. rectus capitis ventralis lateralis.

Tympanic and Temporal Regions

Stapedial Artery and Canal The stapedial artery travels in a groove on the roof of the quadrate, from the area of the siphonial ostium rostrolaterally to a dorsal ridge extending from the dorsal aspect of the quadrate, the exoccipital process of the quadrate. The vessel then enters the external ostium of the stapedial canal (Reese 1914), the entrance of which is formed medially by a notch in the lateral aspect of the exoccipital which is ventral to the medial aspect of the paroccipital 243 process, dorsally by the ventromedial aspect of the paroccipital process, ventrally by the

dorsomedial aspect of the quadrate, and laterally by the above mentioned dorsal ridge of the

quadrate. The notch in the otoccipital is rostrally continuous with a deep, longitudinal,

groove in the lateral aspect of the exoccipital, the stapedial groove, that forms the medial

wall and floor of the stapedial canal. The lateral wall of the canal is formed by a deep groove

across the dorsomedial aspect of the quadrate located between the exoccipital process of the

quadrate laterally, the pterygoid process of the quadrate ventromedially, and the opisthotic

process of the quadrate rostromedially. The caudal quadrate process of the squamosal (the

quadrate articulates with the squamosal in two places) articulates with the lateral aspect of the exoccipital process of the squamosal, and dorsomedially, with the caudodorsal aspect of the paroccipital process. The stapedial artery and vein course rostrally through the stapedial canal toward the rostrodorsomedialmost aspect of the exoccipital. A notch (caudally convex) in the rostral aspect of the exoccipital process of the quadrate leaves the rostral aspect of the stapedial canal laterally open. The internal ostium of the stapedial canal is formed medially and ventrally by the stapedial groove in the rostrodorsolateral aspect of the exoccipital, dorsomedially by the exoccipital, and dorsolaterally by the rostroventral aspect of the caudal quadrate process of the squamosal. The vessels exit the stapedial canal into the middle ear space. The stapedial groove “bifurcates” and becomes continuous ventrally with a rostroventrally oriented groove that runs across the rostromedial aspect of the opisthotic, into which the internal perilymphatic foramen opens, and which ends ventrally in the endocranium. Dorsally, the stapedial groove is continuous with a wide groove that runs across the rostral face of the exoccipital that forms the lateral aspect of the supraoccipital process of the otoccipital. 244 Auricular Artery and Plexus Upon entering the middle ear space, the stapedial artery sends out an array of arteries

that form a dense plexus that appears to be cavernous tissue in the external auditory meatus.

In section, the tissue of the middle ear region is spongy in appearance, similar to narial

erectile tissue, and produces large amounts of blood when squeezed, again like narial erectile tissue. Laterally the erectile plexus spreads throughout the submucosa of the medial surface of the dorsal ear flap. Figure 5 in Shute and Bellairs (1953) is a photomicrograph of the caudal aspect of the dorsal ear flap in transverse section which illustrates the dense vasculature of this tissue. Dorsally, the plexus spreads across the dorsal aspect of the dorsal ear flap and further medially across the aspect of the roof of the middle ear cavity formed by the ventral surface of the postorbital process of the squamosal. Caudomedially, the plexus extends across the caudolateral surface of the otic process of the squamosal.

The stapedial artery then bifurcates into the dorsally inclined temporoorbital artery,

and a rostroventrally oriented vessel(s) that travels along a ridge on the otoccipital, and then

across the subcapsular process, which forms the floor of the fenestra cochleae and

overhangs the ostium for the common encephalic artery. This last vessel then sends out

branches to supply the tympanic membrane, then travels rostrodorsally passing over a shelf

which is continuous with the otoccipital groove, and then courses lateral to the middle

pneumatic fossa in the otoccipital.

Cranioquadrate Canal The temporoorbital artery courses rostrodorsally across the groove in the rostral

face of the exoccipital, dorsal and lateral to the fenestrae cochleae and vestibuli, and the

columella. The vessel then courses rostrally across the dorsal aspect of the opisthotic

process of the prootic. Further rostrally, the vessels pass through the internal ostium of the 245 cranioquadrate canal which is formed ventrally by the dorsal aspect of the prootic, laterally

by a groove in the medial aspect of the quadrate between the quadrate’s squamosal and otic

cotyles, dorsally by the postorbital process of the squamosal, and medially by the

caudodorsolateral aspect of the parietal process of the squamosal. The vessels then travel rostrodorsally through the cranioquadrate canal which shares the same borders as the canal’s internal ostium. The vessels enter the dorsal temporal fossa through the external cranioquadrate ostium, formed medially by the dorsolateral aspect of the parietal, and laterally by the dorsomedial aspect of the squamosal. Throughout its course through the middle ear space from the internal ostium of the cranioquadrate canal to the external ostium of the dorsal cranioquadrate canal, the temporoorbital vascular bundle travels within a thick tube of cartilage-like connective tissue that is confluent with the thick tissue lining the middle ear space.

Anatomy of the Postorbital Region The postorbital region forms an important intersection between the vasculature of

the temporal and orbital regions. Several bony elements in the postorbital region form

osteological correlates for the vessels in this area. Numerous vessels and a large vascular

plexus are intimately associated with the bony orbit. The postorbital bones define important

parts of the orbital cavity, thus forming osteological correlates for the orbital vasculature and

vascular plexus (e.g., it is important to accurately describe the borders of the orbital space

because a large plexus extends across it). Moreover, the postorbital bones (e.g., the

laterosphenoid) possess numerous osteological correlates for orbital and temporal muscles,

many of which are ubiquitous across Archosauria. The vascular supply to these muscles is

quite similar in birds and crocodilians, and the osteological correlates for these muscles may 246 provide an opportunity to reconstruct the pattern and structure of the vessels in this area in

fossil archosaurs.

The rostrodorsal face of the postorbital bone has a thick vertically oriented ridge

along its lateralmost aspect, and medial to this ridge the bone is smooth and characterized by

a rostrally facing fossa that rostrodorsally continues into the ventral aspect of the parietal.

The lateral ridge of the rostrodorsal surface of the postorbital bone is covered by a thick

periosteum confluent with the more medial circumorbital membrane and that continues

caudally across the dorsolateral postorbital bone and finally curves across a fossa in the

caudolateral postorbital bone and forms the rostrolateral border of the external auditory

meatus. The rostrolateral ridge of the postorbital bone defines the caudolateral border of

the orbital margin.

A large crest, the cotylar crest, originates from the medial aspect of the laterosphenoid capitate process (Clarke et al. 1993), curves ventrally (the curve is rostrally convex) and becomes confluent with the rostral aspect of the bar that forms the lateral border of the profundus foramen In addition to the profundus foramen which opens just rostral to the cotylar crest, the trochlear foramen is located rostral to the central area of this crest. The caudomedial circumorbital membrane originates from the lateral aspect of the cotylar crest, that defines the caudomedial orbital margin. The cranial adductor aponeurosis connects to the rostromedial aspect of AME profundus as fibrous connections to the caudal border of the cotylar crest.

Just caudal to the ventral aspect of the cotylar crest is a shallow protuberance, the m.

tensor periorbitae process, into which a caudoventral tendon of m. tensor periorbitae inserts.

This is a laterally oriented process that originates from the ventrolateral aspect of the 247 laterosphenoid. A curved line (concave rostrally) from the laterosphenoid crest to the m. tensor periorbitae process and then from the process to the rostrolateral crest of the postorbital bone (which is steeply dorsolaterally inclined) defines the ventral border of the caudal orbital margin. The circumorbital membrane extends dorsally from this line to the dorsolateral edges of the rostral postorbital and the caudal parietal, and in effect forms the caudal orbital margin. As such, the large space between and also ventral to the sutural contact of the lateral laterosphenoid and the medial postorbital is covered by the circumorbital membrane. The membrane acts to divide the temporal and orbital spaces.

Immediately caudal to the circumorbital membrane are several osteological correlates for various muscles of the temporal region. Across the laterosphenoid are two important processes. Caudal to the dorsal aspect of this cotylar crest, and just ventral to the capitate

(Clarke et al. 1993) process for articulation of the dorsal laterosphenoid with the postorbital bone, is a robust vertically oriented ridge into which an aponeurosis of AME profundus pars rostralis inserts. The muscle can further insert into the fossa between the ridge and the cotylar crest, and into the caudoventral aspect of the cotylar crest (Busbey 1989). Just caudal to the m. tensor periorbitae process, on the bar of the ventral laterosphenoid that forms the lateral border of the profundus foramen, rostral to the maxillomandibular foramen is a second and more robust protuberance, the pseudotemporalis process, from which a thick tendon of m. pseudotemporalis caudodorsally originates. Caudally, a robust protuberance extends laterally from the rostral prootic, just caudal to the prootic-laterosphenoid suture, just dorsal to the maxillomandibular foramen, and caudal to the middle cerebral vein foramen. The protuberance has a long tapering caudal aspect to it, that forms a wide ridge across the middle aspect of the caudal prootic. A tendon of AME medialis inserts into this, 248 the AME medialis process. The AME medialis process is at the ventromedialmost aspect of

the temporal canal.

Osteology of the Temporal Canal As the temporal canal is an osteological correlates for the temporoorbital

vasculature, it will be described here to provide detailed osteological correlates for this vasculature which can be compared to birds.

The temporal canal is formed rostrally by the articulation of the laterosphenoid

cotyle with the ventromedial surface of the postorbital bone. The dorsal laterosphenoid

caudal to the cotylar ridge is characterized by a deep caudodorsally facing fossa that forms

the rostromedial wall of the temporal canal. The caudomedial wall of the temporal canal is

formed by the rostrodorsal surface of the prootic, which has a rostrolaterally facing fossa

that is continuous with the fossa in the laterosphenoid. The AME medialis process, and its

tapering caudal ridge, marks the ventral border of the medial aspect of the temporal canal.

From the dorsal prootic fossa and dorsal to the AME medialis process the prootic extends

caudodorsally to the ventral aspect of the quadrate, then curves rostromedially, forming a

pyramidal shape, across the ventral quadrate before tapering to an apex at the medial

postorbital bone, and nearly contacts the caudal aspect of the laterosphenoid capitate

process. A ventral projecting ridge extends from the apex of the prootic and courses

caudally across the pyramid. The area lateral to this ridge forms the caudolateral border of

the temporal canal, whereas the area medial to the ridge and to the pyramidal eminence

defines the lateral border of the canal. Again, the bone of the lateral border of temporal

canal has a deep fossa that faces medially. The lateral border of the canal is continuous with

the fossa along the prootic that defines the caudomedial aspect of the canal. The contact 249 between the postorbital and laterosphenoid defines the rostral border of the canal. The lateral border of the canal is continuous with the fossa along the prootic that defines the caudomedial aspect of the canal. As such, the entire circumference of the temporal canal is defined by a nearly continuous fossa except at its rostralmost aspect. Moreover, the caudal aspect of the canal is wide and tapers to a more constricted point at the rostral border.

Dorsal to the lateral border of the canal is the medially protruding shelf formed by the medial postorbital and medial squamosal that forms the lateral border of the medial temporal fenestra.

The caudodorsolateral laterosphenoid and the rostrodorsolateral prootic together dorsally articulate with the caudoventromedial surface of the parietal. Across this aspect of the parietal is a thick medially projecting ridge. Ventral to the parietal ridge is a deep laterally facing fossa of the parietal that is ventrally continuous with the fossa of the medial border of the temporal canal, and thus forms the dorsalmost aspect of this border. The medial parietal ridge itself forms the medial border of the medial dorsal temporal fenestra. The parietal ridge extends rostromedially across the curvature of the parietal and then across the postorbital-parietal suture where it becomes confluent with the ridge that defines the lateral border of the medial dorsal temporal fenestra. This laterally, rostrally, and medially confluent system of medially projecting ridges forms the dorsal temporal shelf. The shelf ends, both medially and laterally where the parietal and squamosal meet, dorsal to the prootic and ventral to the rostral ostium of the cranioquadrate canal. The circumference formed by the rostrodorsomedial postorbital and squamosal, the caudodorsomedial squamosal and parietal, and the more rostrodorsolateral parietal and rostrodorsomedial postorbital, defines the lateral dorsal temporal fenestra. The lateral temporal fenestra is both 250 lateral and dorsal to the temporal shelf. The space between the lateral dorsal temporal

fenestra and the medial dorsal temporal fenestra, which is floored by the dorsal temporal

shelf, is the dorsal temporal fossa.

Vasculature of the Dorsal Temporal Fossa The vascular complex of the dorsal temporal fossa is an extremely complex system,

in that the vascular patterns and structures can be quite different between individuals, and

can present asymmetrical patterns and structures in the same individual. However, the more

general patterns and structures of the dorsal temporal vasculature do demonstrate a

consistency of form within and between individuals.

The Lateral Temporoorbital Artery and Vein

Within the cranioquadrate canal, the temporoorbital artery travels along the dorsal aspect of the larger temporoorbital vein. Upon exiting the cranioquadrate canal through the rostral cranioquadrate foramen, and entering the dorsal temporal fossa, the lateral temporoorbital artery immediately forms a loop. The vessel bends rostromedially across the caudodorsal aspect of AME profundus pars caudalis, courses rostromedially, and then sharply curves rostrolaterally across the muscle to the lateral dorsal temporal shelf and the lateral aspect of the muscle. This loop was found in all alligatorid specimens and never demonstrated an asymmetrical pattern. The temporoorbital artery then courses rostrally, and slightly medially, across the curvature (concave medially) of the lateral dorsal temporal shelf, and across the lateral aspect of AME profundus pars caudalis, and sends ventral vessels into the muscle.

The lateral temporoorbital vein, upon entering the cranioquadrate canal along the

lateral aspect of the artery, sharply curves rostromedially with the lateral temporoorbital 251 artery, and forms a loop against the lateral aspect of the arterial loop. The vein then follows closely along the lateral aspect of the artery, and receives a series of veins from the lateral area of AME profundus pars caudalis.

The temporoorbital artery curves rostromedially away form the lateral dorsal temporal shelf, and courses rostrally through the dorsal body of AME profundus pars caudalis, and then bends medially to course medially through the rostral aspect of the muscle. The temporoorbital vein, however, continues to course rostrally across the lateral dorsal temporal shelf. The artery then shifts direction and sharply dives rostroventrally.

At the point the temporoorbital artery originally turns rostromedially to pass through the musculature, the lateral temporoorbital vein sends off a rostral ramus. The rostral ramus is a rostroventrally oriented vessel that travels first ventral and then on the external aspect of the artery through its course.

Further caudally, at the point the artery first reaches the lateral aspect of AME profundus pars caudalis, the lateral temporoorbital vein sends off a caudal ramus. The caudal ramus is a ventromedially oriented vessel that passes under the temporoorbital artery to the artery’s medial aspect, and then courses for a distance along the medial aspect of the artery before turning rostromedially to course through the muscle. Further rostromedially, the caudal ramus of the temporoorbital vein sends of a rostroventral tributary that passes ventral or dorsal to the temporoorbital artery to anastomose with the rostral ramus of the temporoorbital vein. The caudal ramus then bends along the internal aspect of the temporoorbital artery at the artery’s medialmost extent, and sends off a medial vessel that anastomoses with the medial temporoorbital vein, after which the caudal ramus passes along the medial aspect of the artery as it descends rostroventrally. 252 Early in the artery’s descent, it is surrounded by the caudal ramus of the temporoorbital vein on its internal aspect, and the rostral ramus on its external aspect, after which the two veins anastomose to form a single vessel that sends off a dense series of vessels across the artery and forms a plexus across the rostral aspect of the artery. The vascular course through the temporal canal is discussed below.

Medial Temporoorbital Artery and Vein

Before exiting the cranioquadrate canal, the temporoorbital artery gives off a ventrally directed smaller vessel, the medial dorsal temporal artery, which then runs rostrally along the former vessel’s ventral aspect. The medial dorsal temporal vein arises from the medial aspect of the temporoorbital vein as the latter vessel passes through the rostral cranioquadrate canal, and then passes medially under the lateral temporoorbital artery.

After exiting the cranioquadrate canal, the medial dorsal temporal vein curves medially around the caudodorsal aspect of AME profundus pars caudalis, and then passes rostrally along the medial aspect of AME profundus pars caudalis and across the medial aspect of the medial dorsal temporal shelf. In its course, the vein receives a series of dorsomedially oriented veins that drain from the medial area of AME profundus pars caudalis. The medial dorsal temporal artery breaks up into an arterial plexus that courses closely along the lateral aspect of the vein, and in its course sends off a dense array of vessels into the medial aspect of AME profundus pars caudalis. The medial dorsal temporal vein continues to course along the medial dorsal temporal shelf toward the rostral aspect of the dorsal temporal fossa.

Lateral Postorbital Canal and Plexus At the rostral aspect of the dorsal temporal fossa, the medial dorsal temporal vein curves and then courses laterally across the dorsal temporal shelf before meeting and 253 anastomosing with the lateral continuation of the temporoorbital vein. The veins then form a single, long semicircular vein around the dorsal temporal fossa, except for the fossa’s caudal extent. The rostrolateralmost aspect of the semicircular vein sends off a rostrally oriented vein that courses to, and then enters through, the caudolateral postorbital foramen, and then courses through the lateral postorbital canal and exits through the rostrolateral postorbital foramen on the dorsolateral aspect of the postorbital bone. The rostromedialmost aspect of the semicircular vein sends off a large rostrolaterally oriented vein that courses to, and then enters, the caudomedial postorbital foramen and follows a canal system to the lateral aspect of the postorbital.

Both of these veins, the medial and lateral dorsal postorbital veins, can originate from any aspect of the medial dorsal temporal or the temporoorbital veins, rather than exclusively arising from the anastomotic venous ring. There can be a number of different anastomoses between the above two vessels, and the dorsal postorbital veins can also originate from some of the more rostral anastomoses. A similar situation is found with the dorsal postorbital arteries. The lateral postorbital artery is often derived from the rostrolateral aspect of the temporoorbital artery before it turns medially to pass through

AME profundus pars caudalis. The medial postorbital artery can originate from any aspect of the temporoorbital as it passes rostrally through AME profundus pars caudalis. Often, an artery from the medial aspect of the temporoorbital artery will rostrolaterally anastomose with a rostromedially inclined branch of the temporoorbital artery and form an arterial arc

(caudally concave), in a position caudal, rostral, dorsal, or ventral to the rostral venous arc.

Similarly, the dorsal postorbital arteries can course dorsal or ventral to the venous arch en route to the caudal postorbital foramina. These arteries typically pass along the lateral 254 aspects of the dorsal postorbital veins in their course to, through, and out of the postorbital canals.

Upon exiting the rostral postorbital foramina, the dorsal postorbital vessels anastomose and form an extremely dense vascular plexus on the thick periosteum on the dorsolateral aspect of the postorbital bone. This plexus extends ventrally across the postorbital bar and its branches anastomose with branches from a plexiform system of vessels derived from the maxillary vasculature (e.g., the rostral auricular artery) that course dorsally across the postorbital bar. The dorsal aspect of the postorbital plexus extends medially across the rostrolateral postorbital ridge which allows the vessels to pass over to the caudolateral border of the orbit.

The vessels of the enormous postorbital plexus pass medially across the circumorbital membrane as the membrane stretches between the cotylar crest and the rostrolateral ridge of the postorbital and divides the orbital and temporal regions. The plexus extends to anastomose with vessels derived from the caudal rami of the supraorbital artery and vein. Throughout much of this system, the venous plexus is external to an arterial plexus. As a result, the caudal aspect of the orbit contains a single, vast vascular plexus.

Moreover, several large vessels derived from the dorsal postorbital vessels as they exit the postorbital canals, pass rostrally through the plexus and to the ventral aspect of the dorsal palpebra. The dorsal palpebral vessels then ramify throughout the tissue of the dorsal palpebra and form a dense dorsal palpebral plexus, caudally continuous with the postorbital plexus. The dorsal palpebral plexus forms a complex vascular system that extends across and fills the lateral border of the orbit. 255 Vasculature of the Temporal Canal and the Temporal Rete The temporoorbital veins and artery descend rostroventrally through the temporal canal along the rostromedial aspect of AME profundus pars caudalis. Passing further through the temporal canal, the vessels course rostroventrally on the rostromedial aspect of

AME profundus pars rostralis and later on the muscle’s lateral aspect, along the muscle’s rostrodorsalmost extent that reaches to the rostrodorsal area of the temporal canal. Just medial to the sutural area between the laterosphenoid cotyle and the postorbital bone, both the artery and the vein break up into a dense plexus, with the venous plexus resting just lateral to the arterial plexus. The rete is situated against the lateral aspect of AME profundus and the lateral aspect of AME profundus pars caudalis. In this position AME profundus pars caudalis is mainly composed of a thick aponeurosis with only a few muscle fibers mixed in. Rostrally, the aponeurosis of AME profundus pars caudalis becomes confluent with the tendinous rostral aspect of AME profundus pars rostralis to form a thick connective tissue system that is continuous with the cranial adductor aponeurois. The rete extends rostrally into and is suspended by this aponeurotic system formed by AME profundus pars rostralis and caudalis. In this region, the temporoorbital artery and accompanying vein give off branches, the postorbital artery and vein, that pass laterally across the rostral aspect of the fleshy and tendinous rostral aspect of AME profundus pars caudalis and then AME superficialis, and supply and drain the rostral aspects of these muscles.

After giving off the postorbital vessels, the temporoorbital artery and vein again divide into a ventral and dorsal artery and vein, respectively. The ventral vessels are the infraorbital artery and vein. The dorsal vessels are the profundus artery and vein. The profundus vessels course rostrally through the aponeurosis, dorsal to the rete. The rostral aspect of the aponeurosis forms a thick “sleave” that encloses the profundus vasculature 256 rostral to the rete. At its rostralmost extent, the profundus sleeve contacts and becomes confluent with the caudal aspect of the caudomedial border of the circumorbital membrane, through which the vessels pass into the orbit and then divide into the ophthalmotemporal and supraorbital arteries and veins. This aspect of the crocodilian head vasculature is discussed in further detail in the section on the orbital vasculature.

Additionally, near its rostral extent against AME profundus pars caudalis, the lateral temporoorbital vein can give off a ventrolateral vessel that descends along the rostrolateral aspect of AME profundus pars caudalis where the muscle becomes tendinous, and ultimately travels toward the retia, and than sends branches that anastomoses into the rete. Another vein can course rostroventrally from the medial temporoorbital vein, against the medial aspect of AME profundus pars caudalis, and then to AME profundus pars rostralis, after which it sends off more vessels to the venous rete.

Orbital Region

Myology and Osteology of the Orbit The anatomy and vascular relationships of the ocular muscles in crocodilians is quite similar to the avian condition, with some exceptions. Most of these muscles have identifiable osteological correlates (depending on age and the individual) or have cartilaginous correlates associated with the orbital cartilage. The orbital cartilage is variably ossified within

Archosauria, across ontogenetic stages, individuals within a population, and clades.

M. rectus medialis originates from a thick tendon that inserts into a vertically oriented, horizontally compressed, fossa in the orbital cartilage, just rostral to the optic nerve foramen. A thick swelling protruding caudally from the mid-caudal aspect of the prefrontal bone serves as the origin for the two obliquus muscles (Underwood 1970). The tendon of 257 m. obliquus dorsalis originates from the more dorsal aspect of the process, and the tendon of m. obliquus ventralis originates just ventral to the former tendon (Underwood 1970). The tendon of m. rectus ventralis originates from a ridge located along the rostralmost aspect of the laterosphenoid, ventral to the optic tract, and the rectus dorsalis tendon inserts just caudal to this ridge. In birds, mm. rectus ventralis and dorsalis originate from a common ridge, and this is nearly the condition found in crocodilians. The external oculomotor nerve foramen is positioned between the tendinous origins of mm. rectus lateralis and dorsalis, and the profundus nerve passes rostrally between m. rectus dorsalis and m. rectus lateralis early in its course.

The crocodilian abducens musculature is divided into three muscle masses: mm. rectus lateralis, retractor bulbi, and pyramidalis. The tendon of the m. rectus lateralis originates from a lateral projecting, hook-like, process of the laterosphenoid, and protrudes from the rostroventral aspect of the medial wall of the profundus canal. In some specimens the m. rectus lateralis process protrudes far lateral into the external profundus foramen, and nearly meets a medially projecting process on the lateral wall of the foramen, which would divide the external foramen into dorsal and ventral components. The tendon of m. retractor bulbi originates from a variably ossified, knob-like process extending from the bony, wing- like lateral extension of the basisphenoid rostrum (Underwood 1970) ventral to the profundal canal. This wing-like structure has a deep vertical fossa that m. pseudotemporalis partially rests in. The tendon of m. tensor periorbitae originates from the laterosphenoid just ventrolateral to the tendon of the retractor bulbi muscle. M. pyramidalis appears to consist of two bellies, an oblique rostrolaterally oriented belly that travels caudal to the optic nerve and inserts into the eyeball dorsal to the nerve and a horizontally oriented belly that 258 stretches across the circumference of the eyeball (except for the lateral aspect). The horizontal belly is dorsal to the oblique muscle, and is connected to the oblique belly through thick white fibers near the area of insertion of the oblique belly into the eyeball.

After coursing across m. rectus dorsalis, the profundus nerve travels across the dorsal aspect of the ventral belly of m. retractor bulbi. The rostral component of the dorsal belly of m. retractor bulbi passes medial to m. rectus medialis, whereas the caudal component passes medial to m. rectus lateralis.

The tendon of m. levator palpebrae has a horizontal attachment to the median dorsal aspect of the orbital cartilage, but does not have any detectable cartilaginous correlate.

The oculomotor nerve courses rostrally between the ventral aspect of m. rectus dorsalis and the lateral aspect of m. rectus lateralis, and then courses between the ventral aspect of the former muscle and m. rectus ventralis. The abducens nerve and its accompanying vasculature travel rostrally between the dorsal aspect of the m. tensor periorbitae and the ventral aspect of m. rectus ventralis.

Lacrimal Gland The lacrimal gland is located between the ventral palpebra and the nictitating membrane, just rostral to and upon the midline of the eyeball, and is almost completely

“cupped” by the concavity of a fold leading from the ventral palpebra to the nictitating membrane in the ventralmost region between these two tissues. The gland appears as a small, black, and solid structure.

Orbital Vasculature The temporoorbital vein courses rostrally along the dorsal aspect of the temporoorbital artery against the rostrolateral aspect of the laterosphenoid and just ventral 259 to the postorbital condyle of the laterosphenoid. Along the cotylar crest, the temporoorbital artery and vein bifurcate into ventral and dorsal branches, the infraorbital and profundus arteries and veins, respectively.

Just rostral to the cotylar ridge against the caudodorsolateral aspect of the circumorbital membrane, the profundus artery remains in a position ventral and parallel to the profundus vein, and both artery and vein immediately bifurcate into dorsal and ventral branches, the supraorbital and ophthalmotemporal arteries and veins, respectively.

Supraorbital Artery and Vein

The cotylar crest extends from a caudolaterally oriented flexure of the laterosphenoid. The area rostral to this flexure, the rostrolateral aspect of the laterosphenoid, forms a caudolateral to rostromedial oriented sheet of bone that serves as the bony caudomedial aspect of the orbit. The supraorbital artery is given off and proceeds to travel dorsally across the area of the laterosphenoid between the flexure and the obliquely oriented orbital component of the bone. The artery courses dorsally across the lateral aspect of the laterosphenoid-frontal suture, and then travels a short distance to the caudoventrolateral aspect of the frontal. This area of the frontal rostral to the rostrolateral postorbital-frontal suture forms the caudodorsal bony orbital margin. The vessel then travels rostrally and slightly dorsally across the lateral aspect of the frontal, and across the circumference of the bony caudodorsal orbital margin. The vessel’s path is tortuous, with dorsal to ventral, and vise versa, twists throughout the course. Additionally, throughout the artery’s course, the vessel sends off a dense array of ventral vessels that course ventrally and anastomose across the caudal orbital margin and caudal aspect of the circumorbital 260 membrane, forming an extremely dense plexus that is ventrally fed and drained by branches of the orbital artery and vein.

Caudodorsal to the rostralmost aspect of the frontal-laterosphenoid suture, the frontal bones curve and extend rostrally across the orbit to form the dorsomedial bony margin. The supraorbital vessels curve along the frontal and then course across the dorsal aspect of the dorsomedial orbital margin, maintaining their tortuous anatomy. Proximal in this course, the vessels send off and receive anastomotic vessels between the supraorbital artery and vein and the ophthalmotemporal artery and vein. Again, in this region, the supraorbital vessels send off a dense array of ventral branches that course ventrally and anastomose across the medial bony orbital margin and the lateral aspect of the medial circumorbital membrane. In this path, the supraorbital artery sends off dorsally oriented vessels that pass into a series of small foramina, across the orbital aspect of the frontal, and exit through nutrient foramina in the skull roof.

Further rostral along the medial aspect of the orbit, the frontal bone curves rostrolaterally toward the prefrontal bone. This rostralmost aspect of the frontal and the frontal-prefrontal sutural contact form the rostrodorsomedial bony orbital margin. The lateral aspect of the prefrontal forms the rostrodorsal bony orbital margin. Just caudal to the frontal-prefrontal contact, the vessels derived from the supraorbital + ophthalmotemporal anastomosis bifurcate into dorsal and ventral branches. The ventral branch travels ventrally along the caudal surface of the suture to the orbitonasal fenestra and meets with the profundus nerve. In this region, the vessels anastomose with ophthalmotemporal artery and vein derived vessels that supply the rostrodorsal aspect of the Harderian gland. The orbitonasal fenestra is located in the rostrodorsal aspect of the interorbital septum in a 261 position caudoventral to the bony notch formed by the rostrolateral aspect of the frontal and the caudodorsal aspect of the prefrontal pillar. The neurovascular bundle travels rostromedially through the orbitonasal fenestra, and the vessels anastomose with the ethmoid vasculature.

The rostral branch from the supraorbital + ophthalmotemporal anastomosis travels rostroventrolaterally across the prefrontal to the lacrimal foramen (Rathke 1866; Hochstetter

1906). Upon reaching the foramen, the vessels ramify into a dense plexus of vessels that enter into the foramen and travel across all aspects of the nasolacrimal duct. Before passing into the foramen, the artery and its branches anastomose with vessels derived from the facial and dorsal alveolar arteries.

Ophthalmotemporal Artery and Vein

Subsequent to branching from the profundus artery, the ophthalmotemporal artery courses medially across the caudodorsal aspect of m. tensor periorbitae, toward the dorsolateral aspect of m. rectus lateralis.

In its proximal most course, the ophthalmotemporal vein rests against the artery’s dorsal aspect and immediately bifurcates into a dorsal and a much larger ventral rami. The ventral ramus travels rostroventrally across the medial aspect of the artery to the latter vessel’s ventral aspect. The dorsal ramus of the vein courses parallel to and along the dorsal aspect of the artery, whereas the ventral ramus of the vein courses parallel to and along the ventral aspect of the artery. At the lateral aspect of m. rectus lateralis, the ventral ramus of the ophthalmotemporal vein courses rostroventrally away from the ophthalmotemporal artery and proceeds to course along the ventrolateral aspect of m. rectus lateralis. 262 The ophthalmotemporal artery travels rostromedially with the dorsal ramus of the ophthalmotemporal vein across the dorsal aspect of m. rectus lateralis and the m. rectus lateralis process. Just medial to the dorsomedial aspect of m. rectus lateralis, the artery sends off a long, slender branch that courses caudoventrolaterally across and past the medial aspect of m. rectus lateralis to the dorsal aspect of m. tensor periorbitae, and then travels rostrolaterally to the ciliary plexus. The ophthalmotemporal artery then continues to course rostromedially to the lateral aspect of m. retractor bulbi, and then travels across the dorsal aspect of m. retractor bulbi to the lateral aspect of m. rectus dorsalis. At the lateral aspect of m. rectus dorsalis, the artery bifurcates into dorsal and ventral branches. The dorsal branch of the ophthalmotemporal artery travels rostrodorsally across the dorsolateral aspect of m. rectus dorsalis, and then anastomoses with the supraorbital artery.

The ventral branch of the ophthalmotemporal artery travels rostroventrally toward the caudodorsal aspect of m. rectus ventralis and in this path travels across the medial aspect of m. retractor bulbi, the ventral aspect of m. rectus dorsalis, and the caudal aspect of the optic nerve. At the caudodorsal aspect of m. rectus ventralis, along the ventromedial aspect of m. retractor bulbi and the caudoventral aspect of the optic nerve, the ventral branch of the ophthalmotemporal artery bifurcates into dorsal and ventral branches. The ventral branch travels rostroventrally across the caudal aspect of m. rectus ventralis to the muscle’s caudoventral aspect, and then travels rostrally across the ventral surface of the muscle.

Further rostrally, the ventral branch courses toward the caudodorsal aspect of m. obliquus ventralis and sends off a dense array of vessels to the Harderian gland in its path. The dorsal branch travels rostrally across the dorsal aspect of m. rectus ventralis and the ventral aspect of the optic nerve. At the rostrodorsal aspect of the optic nerve, the artery sends off 263 branches that travel across the ventral aspect of m. rectus medialis to the Harderian gland into which the branches ramify. The major continuation of the dorsal branch travels dorsally away from m. rectus ventralis, and then across the rostral aspect of the optic nerve and the caudal aspect of m. rectus medialis, and, further dorsally, travels across the caudal aspect of m. obliquus dorsalis and anastomoses with the supraorbital artery.

The above mentioned ventral branch, and main continuation, of the ophthalmotemporal vein, travels rostrally across the ventral surface of m. rectus lateralis to the ventrolateral aspect of m. retractor bulbi, and then bifurcates into dorsal and ventral branches. The dorsal branch travels rostrodorsally across the dorsolateral aspect of m. retractor bulbi. The ventral branch travels rostroventrally across the ventromedial aspect of m. retractor bulbi to the caudodorsal aspect of m. rectus ventralis, and then bifurcates again into dorsal and ventral rami. This last ventral ramus travels across the ventral aspect of m. rectus ventralis, and rostral to the muscle, the vessel turns and travels dorsally across the rostral aspect of m. rectus ventralis. The rest of this vein’s pathway is described below in reference to the innervation of the Harderian gland. The dorsal ramus travels with branches of the ophthalmotemporal artery rostrally across the dorsal aspect of m. rectus ventralis to the area between the rostroventral aspect of the optic nerve, the rostrodorsal aspect of m. rectus ventralis, and the caudoventral aspect of m. rectus medialis. The dorsal ramus then turns and travels dorsally across the caudal aspect of m. rectus medialis and the rostral aspect of the optic nerve.

The arteries of the ophthalmotemporal artery and vein, together with branches of the supraorbital artery and veins, contribute to a complex vascular plexus that encircles the 264 bulbus oculi. This plexus will be referred to as the ocular plexiform ring in the following

description.

The Ocular Plexiform Ring

A plexus of vessels branching from the supraorbital artery descends rostroventrally across the dorsomedial aspect of the eyeball, then travels across the medial aspect of m. pyramidalis, and subsequent to this travels across the medial aspect of m. retractor bulbi where the vessels of the plexus anastomose with branches of the ophthalmotemporal vessels and form a plexus. Elements of this plexus course to the area between rostral m. rectus lateralis caudally and m. retractor bulbi rostrally, and a particularly thick component of this plexus rests across the caudal surface of the former muscle. The plexus extends to an area caudodorsal to the optic nerve and ventral to m. retractor bulbi, and then extends to an area between the caudoventral aspect of the muscle and the caudodorsal aspect of m. rectus ventralis. Part of the plexus between mm. rectus medialis and ventralis splits across the medial aspect of m. retractor bulbi and extends to the area between m. retractor bulbi and the ventral aspect of m. rectus dorsalis. Thus, the vessels associated with m. rectus dorsalis and vessels associated with m. rectus ventralis are united via a plexiform loop that surrounds m. retractor bulbi.

The venous component of the plexus along the ventral aspect of the optic nerve sends off branches that descend across, in order from dorsal to ventral, m. rectus ventralis, m. obliquus ventralis, m. tensor periorbitae, the maxillary nerve, and finally m. pterygoideus dorsalis, and drain into the maxillary vein. Along the dorsal aspect of m. rectus ventralis, branches from this descending vasculature send off caudal branches that anastomose with vessels in a plexus lateral to m. rectus ventralis that extend from the plexus between mm. 265 lateralis and dorsalis. After giving off their ventral branches, the vessels ventral to the optic

nerve course across the rostral aspect of the optic nerve. Along the rostral optic nerve, the

vessels anastomose with vessels in a plexus between the nerve and the caudal aspect of m.

rectus medialis and give off a series of vessels to the caudal Harderian gland.

Branches from the plexus along the caudal surface of m. rectus lateralis travel across the dorsal surface of m. rectus dorsalis and form another plexus between the muscles.

Elements from this plexus anastomose with vessels along the ventral aspect of m. rectus lateralis that arise from the rostroventral vasculature that ultimately passes around the optic nerve. These vessels then form a plexus between the ventral m. rectus lateralis and the dorsal aspect of m. rectus ventralis. This last plexus sends off vessels that form a plexus between m. rectus ventralis and the dorsal aspect of m. tensor periorbitae. Vessels from the plexus pass then from the area between mm. rectus ventralis and tensor periorbitae across the ventromedial eyeball and give off a branch to the ventromedial ciliary plexus, after which the vessels from the plexus anastomose with vessels from the supraorbital artery into the lacrimal plexus.

The plexus passes caudoventrally, from the dorsal aspect of m. rectus dorsalis, to the

caudal aspect of the muscle and spreads across the muscle belly. A component of the plexus

then spreads medially across m. rectus lateralis and between the caudal aspect of the plexus’

lateral aspect and the rostral aspect of m. rectus dorsalis along the plexus’ medial aspect.

Elements of the plexus then pass rostromedially to lie ventral to the ventral aspect of m.

retractor bulbi and along the dorsal aspect of the optic nerve. Vessels within the plexus then

pass caudoventrally to a position between the caudoventral m. retractor bulbi and the dorsal

aspect of m. rectus ventralis. Some of the vessels in the plexus between mm. retractor bulbi 266 and ventralis pass dorsally across the medial aspect of m. retractor bulbi and the ventral aspect of m. rectus dorsalis, and form a dense anastomotic link between the dense vasculature associated with mm. rectus dorsalis (and thus, the temporal vasculature) and lateralis and m. rectus ventralis (and thus, the ventral ciliary vasculature).

Orbital Artery

The orbital artery travels out of the endocranium through a bony notch formed by the rostroventromedial aspect of the laterosphenoid and the dorsal aspect of the wing off the parabasisphenoid rostrum. The notch is actually patt of a foramen that is dorsally, and partially medially completed by cartilage continuous with the orbitosphenoid cartilage. The foramen is rostromedial to the abducens foramen, and rostroventromedial to the oculomotor foramen. The vessel travels through the orbit to an area lateral to m. rectus dorsalis and caudodorsal to the origin of m. rectus ventralis, and anastomoses with the ophthalmotemporal artery. Lateral to the profundus nerve, the orbital artery ramifies into a series of dorsally and ventrally oriented vessels. The dorsal ramifications consists of a multitude of fairly large and long vessels that pass rostrodorsally on the medial surface of m. rectus dorsalis and the dorsomedial aspect of the optic nerve, and then anastomoses into the caudodorsal ciliary plexus. More lateral vessels derived from the dorsal branch curve rostrally along the dorsomedial aspect of the eyeball and ramify to form the dorsomedial ciliary plexus, and apparently anastomose with branches from the supraorbital artery. The majority of the more ventral ramifications, which comprise the ventral ciliary artery(ies), passes ventral to the optic tract and contributes to a ventrally oriented plexus situated between the dorsal aspect of m. rectus ventralis and the ventral aspect of the eyeball. 267 Harderian Gland The medial component of the main body of the Harderian gland in crocodilians sits along the rostromedial aspect of the eyeball, and caudally tapers to a globular tail wear the median section of the medial aspect of the eye. This aspect of the Harderian gland lies medial to the medial rectus as the muscle inserts into the eyeball. The gland is obliquely crossed along it rostrodorsal aspect by m. rectus obliquus dorsalis, and obliquely crossed along its rostroventral aspect by m. obliquus ventralis. The tail is situated just rostral to the optic nerve and is dorsal to the muscle body of m. rectus ventralis.

Rostral Ramus of the Trigeminal Artery The rostral ramus of the trigeminal artery travels rostroventrally through the profundus canal, along the medial surface of the canal’s floor. Before exiting to the orbit through the external profundus foramen, the artery bifurcates into medial and lateral branches. The medial and larger branch travels rostrodorsomedially toward the ophthalmotemporal artery, and in this course sends off a ventral branch that courses into the external abducens foramen along the exiting abducens nerve. Further rostrodorsally, the artery terminates by joining the ophthalmotemporal artery just before the latter vessel anastomoses with the orbital artery.

The lateral branch of the rostral ramus of the trigeminal artery travels laterally across the ventral aspect of the external profundus foramen, and along the lateralmost aspect of the foramen the artery ramifies into several vessels. The largest, and more significant, branch travels ventrally, away from the foramen, across the lateral aspect of the m. retractor bulbi process. The vessel then travels ventrally along the basisphenoid rostrum and across the medial aspect of m. pseudotemporalis, and anastomoses with the sphenoid artery as the

latter vessel emerges from the slit-like external opening of the CN VIIp canal. The result of 268 the sphenoid-trigeminal artery anastomosis is a large vessel that courses rostrolaterally, with

CN VIIp, from the opening of the CN VIIp canal. Proximal in its course, this artery sends

off a small branch that travels rostrodorsally, in a curved path, along the parasphenoid

rostrum, and then travels rostrally across the dorsal surface of the rostrum. After sending

off the artery to the parasphenoid rostrum, the sphenoid-trigeminal artery and CN VIIp travel through a short canal formed by connective tissue dorsally and the sutural region between the dorsomedial aspect of the pterygoid and the rostroventral surface of the

basisphenoid rostrum. Upon emerging from this last canal, CN VIIp and its accompanying

artery enter into the caudomedial aspect of the infraorbital space, and travel rostrolaterally

across the dorsal aspect of the pterygoid and then both nerve and artery bifurcate into caudal

and rostral branches. The caudal branch travels rostrolaterally toward the caudal border of

the suborbital fenestra, whereas the rostral branch courses across the dorsolateral aspect of

the pterygoid and further rostrally across the dorsal aspect of the palatine in a position

medial and parallel to the medial border of the suborbital fenestra. Through their paths, the

sphenoid-trigeminal artery and its branches travel along the medial surface of CN VIIp and its branches.

A second branch of the rostral ramus of the trigeminal artery travels laterally away

from the profundus foramen, across the rostral aspect of the bar that forms the lateral

border of the foramen, and sends branches to the caudal aspect of m. levator periorbitae. A

third branch of the rostral ramus travels dorsally across and past the inner rostral aspect of

the lateral wall of the profundus foramen, then travels dorsally across the laterosphenoid,

and finally anastomoses with the ophthalmotemporal artery in the latter vessel’s proximal

course. 269 Shiino (1914) and Hochstetter (1906) described the trigeminal artery as a branch of the orbital artery rather than the encephalic vasculature. According to these authors, the trigeminal artery travels caudally from the orbital artery and along the profundus artery to the maxillomandibular ganglion, after which the vessels courses laterally with the maxillomandibular nerves to the lateral temporal space where the vessel supplies the adductor musculature. Moreover, these authors describe the terminal branch of the trigeminal artery as traveling with the mandibular nerve into the pterygoideus musculature.

Our observations are quite similar to the above authors. However, I recognized a significant

relationship of the trigeminal artery with the encephalic arterial system. Moreover, in birds,

the encephalic vasculature is the primary blood source to the trigeminal artery.

It is important to note here that in its course through the CN VIIp canal and toward

its exit into the area between the orbit and the infraorbital regions, the sphenoid artery

travels along the medial aspect of the large CN VIIp, and a smaller nerve appears to travel

along the lateral aspect of the larger nerve. It is possible that the smaller nerve represents

the avian dorsal ramus of CN VIIp that travels to the orbit and synapses in the

pterygopalatine ganglion, and that the larger branch represents the avian ventral ramus of

CN VIIp that travels to and innervates the glands of the palate. The branch of the trigeminal

artery that anastomoses with the sphenoid artery could then, alternatively, be viewed as a

dorsal branch of the sphenoid artery that anastomoses with the trigeminal artery and is then

analogous to the sphenomaxillary artery, based on its relationship to the smaller branch of

CN VIIp discussed below. The artery that courses to the infraorbital space with the larger

branch of CN VIIp would then be analogous to the sphenopalatine artery. However, as mentioned above, in its descent across the basisphenoid, CN VIIp is accompanied by two 270 small arteries, and these may be homologous to the avian sphenopalatine and

sphenomaxillary arteries which may (or may not) anastomose in the crocodilian CN VIIp

canal. The problem with this speculation is that this vascular area was notoriously poorly

filled by injection media in all our specimens, and the vessels are extremely small; so any

conclusion may be biased by poor filling.

Upon exiting the CN VIIp canal, the larger branch of CN VIIp appears to send off

branches that “jump” onto and travel along the branches of the trigeminal artery that

ultimately anastomose with the sphenoid artery. Moreover, the smaller branch of CN VIIp appears to “jump” onto the ventral anastomotic branch of the lateral branch of the rostral ramus of the trigeminal artery, and a nerve was seen to course dorsally to the orbit by traveling along this artery. Within the orbit, the nerve appears to sends off branches that

“jump” onto the other vessels derived from rostral ramus of the trigeminal artery.

The branch of the mandibular nerve that innervates m. tensor periorbitae travels

along the lateral aspect of the profundus canal, lateral to the profundus nerve. An

apparently CN VIIp derived nerve travels dorsally on the dorsal artery that travels along the

lateral wall of the profundus foramen. In its course, the artery travels across the lateral

aspect of the branch of the mandibular nerve, and the CN VIIp derived nerve appears to

send off medial branches that “jump” onto the mandibular ramus. Further rostrolaterally,

this mandibular ramus appears to have connections with the abducens nerve. It is quite

possible that branches of CN VIIp travel along the arteries to the abducens foramen and then

directly join the abducens nerve. Based on the observations discussed below, the abducens

nerve seems to be the primary source of nerves that ultimately reach the Harderian gland. 271 Palatine Ramus of the Facial Nerve

The abducens nerve and apparently a branch of the dorsal ramus of CN VIIp travel rostrodorsally to the caudomedial aspect of the fleshy m. retractor bulbi. The abducens nerve then courses rostrodorsally across the caudal aspect of m. retractor bulbi, toward the caudodorsal aspect of this muscle. At the caudodorsal aspect of m. retractor bulbi the abducens nerve appears to divides into small dorsal and ventral branches. These branches travel to tissues not associated with the abducent musculature; they are likely divisions of CN

VIIp, and will be described as such.

Ventral Division of the Dorsal Ramus of CN VIIp

The ventral division travels rostroventrally around the rostroventral aspect of m.

retractor bulbi, and then courses rostrolaterally across the ventral aspect of the muscle

toward the ophthalmotemporal vein.

The ophthalmotemporal vein courses medially toward the medial aspect of the orbit,

and passes through an area between the rostroventral aspect of m. retractor bulb, the

caudoventromedial aspect of m. rectus ventralis, and the caudodorsal aspect of m. tensor

periorbitae. In this area, the vein ramifies into a venous plexus. Further medially, in an area

just rostral to m. retractor bulbi, and ventral to m. rectus ventralis, the venous plexus sends

of a dorsal branch that courses across the rostral aspect of m. retractor bulbi and then

courses caudally across the dorsal aspect of m. retractor bulbi and the ventral aspect of m.

rectus ventralis. This vessel then courses dorsally across the caudal aspect of the latter

muscle and the rostromedial aspect of the tendinous and fleshy components of m. rectus

lateralis, and finally courses rostrodorsally across the caudodorsal aspect of m. rectus

ventralis and joins a plexus situated between this muscle and the caudoventral aspect of the

optic nerve. 272 As the dorsal branch of the palatine nerve approaches the area where the ophthalmotemporal vein passes between mm. rectus ventralis, retractor bulbi, and tensor periorbitae, the nerve turns rostrally and courses to the medial aspect of the ophthalmotemporal veins. The nerve then travels rostrally along the medial aspect of the veins as these veins pass between the ventral aspect of m. rectus ventralis and the dorsal aspect of m. tensor periorbitae. Again, between these two muscles, the veins ramify into a plexus.

The oculomotor nerve enters this area by coursing rostromedially across the dorsal aspect of the tendon of m. rectus lateralis. The nerve then courses across the caudodorsal aspect of m. tensor periorbitae toward the caudoventral aspect of m. rectus ventralis, and travels medial to the branch of the ophthalmotemporal vein that connects the optic nerve-m. rectus ventralis plexus with the m. rectus ventralis-m. tensor periorbitae plexus. The nerve then travels rostrally across the ventral aspect of m. rectus ventralis and along the medial aspect of the ophthalmotemporal vein.

The caudoventromedialmost aspect of the Harderian gland forms a “tail” which is located ventral to the ophthalmotemporal vein, as the vein rests against the rostroventral aspect of m. rectus ventralis. Just rostral to the rostroventral aspect of m. rectus ventralis, the vein curves rostrodorsally and then courses in this direction across the dorsal aspect of the Harderian gland tail, the rostral aspect of m. rectus ventralis, and the caudal aspect of the main body of the Harderian gland. Near the ventral aspect of m. rectus medialis, the vein bifurcates into dorsal and ventral branches. The dorsal branch courses caudodorsally between the rostral aspect of the optic nerve and the dorsomedial aspect of m. rectus medialis. The rostral branch of the ophthalmotemporal vein courses rostrally between the 273 rostroventral aspect of m. rectus medialis and the dorsal aspect of the body of the Harderian gland. Just rostral to the latter muscle, the ophthalmotemporal vein again divides into a dorsal branch that courses across the rostral aspect of m. rectus medialis and then across the medial aspect of the profundus nerve, and a large ventral branch that courses and ramifies across and then into the dorsal aspect of the body of the Harderian gland.

In the area just rostral to m. rectus ventralis, the palatine nerve branch traveling with the ophthalmotemporal vein develops a series of structures that appear from gross observation to be ganglia. These structures will be referred to as ganglia below. However, a histological analysis is necessary to determine if these structures truly are ganglia. The ganglia are positioned along the dorsal aspect of the Harderian gland tail. Fine branches emanating from these ganglia course dorsomedially and join with the oculomotor nerve.

The oculomotor nerve then bifurcates into ventral and dorsal divisions. The palatine nerve gives off ventral branches into the Harderian gland tail, and then the nerve continues to travel along the medial aspect of the ophthalmotemporal vein in the vein’s dorsal course, passing across the lateral aspect of the ventral division of the oculomotor nerve, and then on to the bifurcation of the ophthalmotemporal vein. The ventral division of the oculomotor nerve courses rostroventrally, across the ophthalmotemporal vein. The nerve then travels across the medial and ventromedial aspects of the Harderian gland, and then into m. obliquus ventralis in an area ventral to the Harderian gland. The dorsal division of the oculomotor travels rostrodorsally across the medial aspect of the trunk of the branch of the ophthalmotemporal vein that passes between mm. ventralis and medialis, then courses across the rostral aspect of m. medialis and innervates it, then passes rostrodorsally across the medial aspect of the profundus nerve, and finally passes into m. obliquus dorsalis. 274 At the bifurcation of the ophthalmotemporal vein, the palatine nerve generates a

second series of ganglia, near the caudodorsal aspect of the body of the Harderian gland, and

sends off fine dorsal branches to the dorsal division of the oculomotor nerve. A long, fine

branch emanating from the area of these ganglia courses caudally along the dorsal aspect of

the ventral ramus of the oculomotor nerve, and then turns sharply to course caudodorsally,

first across the medial aspect of the dorsal division of the oculomotor nerve, then across the

medial aspect of the dorsal branch of the ophthalmotemporal vein. The branch then runs

caudodorsomedially across the rostromedial aspect of the optic nerve to the vascular plexus

surrounding the nerve and dorsal to m. rectus ventralis that is partially derived from the

ophthalmic vein. This branch is characterized by a series of ganglia in its proximal course.

The primary continuation of the palatine nerve rostral to the ganglia travels

rostrodorsally along the medial aspect of the ventral branch of the ophthalmotemporal vein.

Just caudal to where this vein bifurcates again into dorsal (to mm. medialis and obliquus

dorsalis) and rostral (to the Harderian gland) branches, on the dorsal aspect of the Harderian

gland, the palatine nerve is characterized by a large ganglion. Fine caudodorsally inclined

branches emanate from the ganglion to the dorsal oculomotor division against m. rectus medialis. A network of fine branches connects the profundus nerve to the ganglion. The main branch off the ganglion courses dorsally along the dorsal branch of the ophthalmotemporal vein.

The rostral branch of the ophthalmotemporal vein continues to travel along the

rostrodorsomedial aspect of the Harderian gland, sending branches into it, and then curves

rostroventrally across the gland to the gland’s rostroventromedial aspect. The vein then

travels laterally across the rostroventral aspect of the gland and the rostrodorsal aspect of m. 275 tensor periorbitae. Further lateral, the vein receives tributaries from a plexus draining the rostral periorbital fascia, and then passes through the ventrolateral periorbital fascia, and finally drains into the rostral aspect of the ventrolateral venous plexus. Veins in the rostral area of this plexus can send off tributaries that drain ventrally into the maxillary vein.

Dorsal Division of the Dorsal Ramus of CN VIIp

The dorsal division of the palatine nerve travels rostrodorsally across the caudal aspect of m. rectus ventralis with the branch of the ophthalmotemporal vein that connects the optic nerve-m. rectus ventralis plexus with the m. rectus ventralis-m. tensor periorbitae plexus. Dorsal to the caudal aspect of m. rectus ventralis, the nerve travels to the ventral aspect of the optic nerve, and continues to travel rostrolaterally across the nerve to the eyeball.

Lateral Temporal Space and Mandible

Osteology and Myology of the Lateral Temporal Space For reasons to be discussed elsewhere, Holliday and Sedlmayr (in prep.) believe the muscle masses originating on the quadrate in crocodilians (which include adductor mandibulae externus superficialis and media, and adductor mandibulae caudalis) and birds

(which include adductor mandibulae caudalis, pseudotemporalis profundus, and m. ossis quadrati) to be homologous. Additionally we believe the muscle masses originating from the squamosal in crocodilians (AME profundus) and birds (AME rostralis and caudalis) to be homologous, and we believe the crocodilian pseudotemporalis and avian pseudotemporalis, which originate from the laterosphenoid, to be homolougs.

Upon emerging from the maxillomandibular foramen, the mandibular nerve passes rostroventrally in a position rostral to m. pterygoideus ventralis, dorsal to the m. 276 pterygoideus dorsalis, and medial to the AME profundus pars rostralis. An early, caudally directed branch travels between two horizontally oriented muscle slips of the m. pterygoideus ventralis, and sends ventral and dorsal nerves to them. The nerve then passes laterally, across the dorsal aspect of the m. pterygoideus dorsalis, and ventral to AME medialis and superficialis, in a region where the latter two muscles approach each other.

The AME medialis process is a large rugose protuberance dorsal to the maxillomandibular foramen and caudodorsal to a small foramen that transmits the trigeminal vein and the nerve to AME profundus, pseudotemporalis, and tensor periorbitae. The process extends from the bone of the caudoventral surface of the prootic process of the quadrate, dorsal to the trigeminal foramen, the ventral sutural contact of the quadrate and prootic, and the ventral aspect of the prootic process of the quadrate. The process continues as a thick caudally tapering ridge that extends across the prootic process of the quadrate and curves caudodorsally across the rostroventral prootic process of the quadrate to the dorsolateral aspect of the mandibular process of the quadrate, where the ridge becomes confluent with the AME superficialis process, another roughened protuberance.

Caudoventral to the AME superficialis process, extending from the rostromedial aspect of the quadrate mandibular process, is another robust protuberance, the AM caudalis crest. A thick ridge, the AM caudalis crest, extends rostroventrally from this process, across the length of the pterygoid process of the quadrate and into and across the dorsal aspect of the quadrate process of the pterygoid. The AM caudalis process is continuous with another ridge that travels caudolaterally from the process and then across the central aspect of the mandibular process of the quadrate. A strong, caudolaterally oriented tendon inserts along the length of the AM caudalis crest. A separate, fleshy, muscle body originates from the 277 caudal and the rostral aspects of the tendon. The tendon extends far laterally as a wide

aponeurosis and continues to divide AM caudalis across much of the muscle’s length. The

aponeurosis ends in the vicinity of the caudoventrolateral aspect of AM caudalis, where the

two muscle bodies blend together and fuse into a single muscle. The nerve of AM caudalis

travels caudomedially after branching from the mandibular nerve toward the AM caudalis

tendon. The nerve then travels rostrally across the tendon and then through the aponeurosis

and gives off nerves to both the medial and lateral muscle bellies in its course. The AM

caudalis artery and vein travel with the nerve, sending branches into (or receiving branches

from) the musculature.

Lateral Ramus of the Trigeminal Artery The encephalic aspect of the trigeminal foramen is walled over by a thick, potentially

dural, connective tissue with several small perforations that allow for the exit of nerves and blood vessels. Similarly the external aspect of the maxillomandibular foramen is walled over by a perforated connective tissue. The lateral ramus of the trigeminal artery passes into the medialmost aspect of the lateral temporal fossa, from the endocranium, through the rostroventralmost perforation in the wall of the maxillomandibular foramen. The lateral ramus of the temporal artery is the most important blood source to the medial aspects of the adductor musculature. The trigeminal vein enters the encephalic cavity from the lateral temporal fossa through a perforation in the mid-ventral aspect of the maxillomandibular foramen, caudal to the trigeminal artery. The vein receives tributaries that travel with the branches of the trigeminal artery. The branches of the lateral ramus ultimately follow along muscular branches of the mandibular nerve to and through the target muscles. After exiting 278 the foramen, the artery courses laterally and then divides into a rostral and caudal branches,

the rostral and caudal trigeminal arteries.

The rostral trigeminal artery travels rostrolaterally and then divides into rostral and

caudal rami. The rostral ramus courses rostrolaterally and then divides into dorsal and

ventral rami. The dorsal ramus travels rostrodorsally and anastomoses with the temporal

artery. The ventral ramus passes rostrolaterally through, and in its course supplies, m.

pseudotemporalis.

The caudal ramus of the rostral trigeminal artery travels laterally through, and in its

course sends off vessels that supply, AME medialis. The vessel then further divides into rostral and caudal rami. The medial ramus courses laterally through and supplies AME medialis and then AME superficialis. The rostral ramus meets with the mandibular nerve and travels rostrolaterally along the nerve’s dorsal aspect between m. pterygoideus dorsalis and m. pseudotemporalis. This rostral ramus terminates as the intramandibular nerve and anastomoses with the ventral alveolar nerve.

The caudal trigeminal artery courses caudoventrolaterally through AME medialis,

and then through AM caudalis, and then curves rostrally to travel rostrally through the

caudal aspect of AME superficialis. A third vessels can branch either directly from the trigeminal artery, a branch of the rostral trigeminal artery, or from the caudal trigeminal artery. This vessel courses caudomedially to and then through m. pterygoideus ventralis, along the nerve to this muscle.

At the rostroventromedialmost aspect of the articular process of the quadrate, along

the medial condyle, the common maxillomandibular artery gives off a medial branch, the

pterygoid artery. The artery courses rostromedially across the rostromedially curved medial 279 aspect of the articular process. In this course, the artery travels between the dorsomedial

aspect of AM caudalis and the dorsolateral aspect of m. pterygoideus ventralis. The artery

then courses rostroventromedially across the caudodorsomedial aspect of the pterygoid

process of the quadrate, just rostrolateral to the process’ contact with the exoccipital bone.

The vessel continues to pass rostroventrally across the pterygoid process of the quadrate.

Temporal Artery Within the rostral aspect of the temporal canal, proximal to sending of the

profundus artery, the temporoorbital artery gives off a large caudally directed vessel, the

temporal artery, which sends off a series of vessels through AME profundus pars caudalis in

its course. Moreover, the temporoorbital artery sends off a series of small vessels that travel

rostrodorsally, lateral to the laterosphenoid bone, and across the lateral aspect of AME

profundus pars rostralis. Caudal to the temporoorbital plexus, and medial to the sutural

contact between the postorbital and laterosphenoid bones, these vessels anastomose with

the rostroventral aspect of the temporoorbital artery. The temporal artery courses

caudoventrally and meets with the dorsal ramus of the AME profundus pars rostralis nerve,

and subsequently travels caudoventrally along the lateral aspect of this nerve toward the

maxillomandibular foramen. Another artery travels caudally along the lateral aspect of the rostral ramus of the AME profundus pars rostralis nerve to the point where the nerve divides into its dorsal and rostral rami. Before this point, both of the arteries traveled across the lateral aspect of AME profundus pars rostralis and the medial aspect of AME medialis.

At the nerve’s bifurcation the temporal artery anastomoses with the artery of the rostral ramus and forms one large vessel that then travels caudoventrally along the AME profundus nerve. The nerve and artery curve caudoventrally around the rostral aspect of the AME 280 medialis process, and then travel caudally across the process’ ventral surface near the maxillomandibular foramen. Just rostral to the foramen, the temporal artery anastomoses with the rostral trigeminal artery.

Trigeminal Vein The trigeminal vein exits the caudodorsal aspect of the external maxillomandibular foramen ventral to the AME medialis process. The vein courses caudally across the ventral aspect of the AME medialis crest, and then across the dorsal aspect of the AM caudalis process. After arriving at the AM caudalis process, the trigeminal vein follows along the path of the pterygoid artery. Just caudal to the AM caudalis process, the vein receives several tributaries that drain AM caudalis and travel dorsally along the caudal aspect of the

AM caudalis crest, and further receives a series of veins that drain dorsally from the AM caudalis vein which drains most of this muscle. Just rostral to the process, the trigeminal vein receives vessels that drain dorsally across the rostral aspect of the AM caudalis ridge.

The vein then courses caudally across the rostroventromedial area of the quadrate between the mandibular process and the dorsal aspect of the pterygoid process. At its caudal extent, the trigeminal vein receives a vein draining from the dorsal surface of the pterygoid and that then courses caudodorsally across the pterygoid process of the quadrate. The pterygoid vein then drains, along the caudoventromedial mandibular process into the maxillomandibular vein and forms the temporomandibular vein. The temporomandibular vein ultimately joins the stapedial vein and the lateral branch of the foramen magnum sinus.

A small foramen is located dorsal to the rostral aspect of the external maxillomandibular foramen. The foramen is formed by the laterosphenoid rostrally and rostrodorsally, and a caudally directed process of the laterosphenoid that forms the ventral 281 floor. The process occasionally contacts the rostroventral aspect of the “orbital” process of the quadrate, usually along the ventral aspect of the AME medialis process. In many specimens, the foramen is not complete and appears as a notch, and in other specimens the foramen is completed by a cartilaginous extension of the process. A similar foramen is found in several fossil non-eusuchian suchians (e.g., sphenosuchids and aetosaurs). The foramen transmits a branch of the mandibular nerve (referred to as the fourth trigeminal nerve) that travels rostrolaterally and innervates the AME profundus muscle. Also traveling through this foramen is a dorsal branch from the complex of trigeminal veins passing through the external maxillomandibular foramen.

In the caudodorsolateral surface of the external maxillomandibular fossa is a rostroventrally facing foramen within the dorsolateral aspect of the prootic. A branch of the venous system passing into the maxillomandibular foramen travels caudodorsally to enter the foramen. The vessel then courses caudodorsally through the prootic, and exits through a foramen in the caudodorsal aspect of the prootic into the rostromedial aspect of the middle ear space. The vessel then travels caudodorsally into the space and ramifies into branches that contribute to the cavernous plexus of the middle ear region.

Temporomandibular Artery The temporomandibular artery passes rostroventral to the caudomedial face of the articular process of the quadrate, enters the caudomedial lateral temporal fossa, and travels rostroventrally to the mandibular joint capsule. The artery then bifurcates into medial and lateral branches, the pterygoid and maxillomandibular arteries, respectively. 282 Pterygoid Artery At the rostroventromedial aspect of the mandibular process of the quadrate before the bone turns ventrally into the pterygoid process, the pterygoid artery bifurcates into dorsal and ventral branches. The dorsal ramus travels toward the AM caudalis process, and courses rostrally across the area of the quadrate that acts as both the rostromedial aspect of the mandibular process and the dorsal aspect of the pterygoid process. Upon reaching the caudal aspect of the AM caudalis process, the artery bifurcates into dorsal and rostral branches. The ventral branch courses ventrally across the caudal aspect of the AM caudalis crest, and gives off branches that supply the caudal body of AM caudalis. The dorsal branch passes rostrally over the dorsal aspect of the AM caudalis process, tendon, and rostral muscle belly. On the rostrodorsomedial aspect of the muscle body, the artery turns ventrally and descends across the rostromedial aspect of the muscle until it intersects with the AM caudalis nerve and artery and anastomoses with the artery.

The ventral ramus of the pterygoid artery courses ventrally along the caudalmost aspect of the pterygoid process of the quadrate, just rostral to the quadrate’s sutural contact with the exoccipital. Further ventrally, the artery courses across the caudodorsolateral quadrate-basioccipital suture, and then crosses to the lateral aspect of the basioccipital. In this area, the lateral aspect of the basioccipital actually serves as a semi-lunar fossa that is dorsally, rostrally, and ventrally bordered by the more laterally protruding caudal aspect of the pterygoid process of the quadrate and, more ventrally, the quadrate process of the pterygoid. The caudolateral aspects of these two processes form an arc-like ridge (caudally concave) rostral to the basioccipital. The dorsal, fleshy, muscle body of m. pterygoideus ventralis fills the fossa. The ventral ramus of the pterygoid artery forms a dense vascular plexus across the basioccipital fossa, and the medial aspect of m. pterygoideus ventralis. 283 Rostroventrally, the plexus extends across the lateral pterygoid-basioccipital suture and the

ventral aspect of m. pterygoideus ventralis, and then spreads rostrally and laterally across the

dorsal surface of the pterygoid bone. Rostrally, the plexus ramifies ventral to m.

pterygoideus dorsalis, and anastomoses with vessels derived from the sphenoid artery (the

“sphenomaxillary” branch).

Maxillomandibular Artery The maxillomandibular artery travels rostrally across the rostromedial aspect of the

quadrate-articular joint capsule, between the rostroventromedial surface of the medial

condyle of the quadrate and the rostrodorsomedial articular bone. In this area, the vessel

first courses rostral to and then across the caudodorsolateral aspect of AM caudalis where a

tendon of the muscle ventrally inserts into the rostral aspect of the internal mandibular

process in the rostromedial aspect of the articular bone. A tendon of m. pterygoideus

ventralis attaches to the caudal aspect of this ridge and the muscle fills a fossa in the

caudomedial articular bone, just caudal to the ridge. Lateral to AM caudalis, the vessels

course along the caudodorsal aspect of AME medialis. At the rostrolateralmost aspect of

the mandibular joint capsule, in the area of the lateral condyle of the quadrate, the

maxillomandibular vessels divide into dorsal and ventral branches, the maxillary and

mandibular arteries and veins.

Mandibular Artery At the rostrolateralmost aspect of the mandibular joint capsule, the

maxillomandibular artery divides into its two largest branches, the mandibular and maxillary

arteries. The mandibular artery is a ventrally directed vessel that originally descends between the caudolateral aspect of AME medialis which is rostral to the vessel, the lateral aspect of 284 AME caudalis which is caudomedial to the artery, and the medial aspect of AME

superficialis which is rostrolateral to the artery. In this course, the artery travels ventral to

the rostroventral aspect of the joint capsule.

The mandibular artery then descends rostroventrally (Rathke 1866; Hochstetter

1906) within a groove situated between the rostromedial aspect of the articular bone and the

caudomedial aspect of the surangular. The groove leads rostroventrally into the caudal

aspect of the mandibular fossa and to a deep confluent groove in the floor of the mandibular fossa, across the caudoventromedial surface of angular. In its ventral course to the floor of the mandibular fossa, the mandibular artery courses between the tendons of the caudoventrolateral aspects of mAM caudalis, pterygoideus ventralis, and AME medialis. On the caudal aspect of the floor of the fossa, the artery then divides into ventral and dorsal rami, the latter of which courses rostrally across the dorsolateral aspect of AME medialis and the length of the external mandibular fenestra.

The ventral ramus of the mandibular artery then courses ventrally along the

curvature of the caudomedial aspect of the external mandibular fenestra, along the

caudolateral aspect of AME medialis, and lateral to AME caudalis and the tendon of m.

pterygoideus dorsalis. In the rostroventral area of the caudal curvature of the external

mandibular fenestra, the mandibular artery and vein both divide into two vessels. The two

venous branches travel dorsal and parallel to the two arterial branches. These four vessels

course rostrally across and then beyond the ventromedial aspect of the external mandibular

fenestra, and along and past the medial aspect of AME medialis (which attaches along the

caudoventrolateral aspect of the fenestra), and lateral to the tendon of m. pterygoideus

dorsalis (which attaches along the caudoventromedial of the internal mandibular fenestra). 285 At the rostral aspect of the external mandibular fenestra and the caudoventrolateral

aspect of m. intramandibularis, the vessels separate. The dorsal artery and vein, the ventral

alveolar artery and vein, travel rostrodorsally through the caudolateral m. intramandibularis,

pass medially across the ventral ramus of the mandibular nerve, and then travel medially

across the dorsal alveolar nerve (Rathke 1866; Hochstetter 1906). Ultimately, the ventral

alveolar vessels arrive at a position dorsal to the ventral alveolar nerve and continue to travel

with the nerve in this position. The ventral alveolar artery gives off a larger branch that

courses ventrally to anastomose with the intramandibular artery.

The ventral vessels, the intramandibular artery and vein, rest on the floor of the

internal aspect of the dentary, lateral to m. intramandibularis, and just ventral to Meckell’s cartilage. The artery gives off dorsal branches that cross dorsolaterally across the intramandibularis muscle. Towards the area where the dentary and m. intramandibularis begin to rostrally taper (along the 14th dentary tooth), the ventral alveolar artery gives off a

series of dorsally oriented arteries that anastomose with a series of ventrally oriented arteries

from the intramandibular artery. Further rostrally, the dorsal alveolar artery courses

rostrodorsally and becomes much smaller in diameter, and the intramandibular artery

courses rostroventrally. Ultimately, the two vessels anastomose and form the rostral

mandibular artery.

Ventral Branches of the Mandibular Nerve The mandibular nerve courses laterally across the caudal face of the rostral aspect of the rostral adductor aponeurosis. The ventrocaudal aspect of this aponeurosis forms a sheet that covers the dorsal aspect of m. pterygoideus dorsalis, and more laterally becomes confluent with the tendon of this muscle. Further lateral, the nerve travels rostrolaterally 286 across m. pterygoideus dorsalis and sends off a ventral branch that travels to the lateral

aspect of the ventral palpebra (Rathke 1866; Hochstetter 1906). The nerve then bifurcates

into a caudal and rostral branches. The caudal branch travels rostrally and passes into the

adductor musculature. The rostral branch travels rostroventrally and then turns laterally to

course to and then through the internal mandibular fenestra and into the mandible. The

mandibular nerve then curves rostrally across the tendon of m. pterygoideus dorsalis, and

then laterally across the caudodorsal aspect of m. intramandibularis. The mandibular nerve

immediately breaks up into two rami, a ventral ramus, and a rostrodorsal branch, the ventral

alveolar nerve.

The ventral ramus of the mandibular nerve travels through the caudal m.

intramandibularis, and near its ventral aspect the vessels divides into rostral and caudal

branches. The caudal branch continues to pass through the ventral m. intramandibularis,

and at the dorsal face of the angular bone. This aspect of the bone contains several small

nutrient foramina, and often a larger rostral and a larger medial foramen. The caudal branch

of the ventral ramus of the mandibular nerve sends off a series of nerves that travel through

the nutrient foramina. The caudal branch of the ventral ramus of the mandibular nerve

usually terminates by splitting into larger rostral and caudal branches, which pass through the

larger rostral and medial angular foramina, respectively.

The rostral branch of the ventral ramus, the intramandibular nerve, courses

rostroventrally through m. intramandibularis, and then courses rostrally through the

ventralmost aspect of the muscle, ventral to Meckel’s cartilage, and passes medially across the intramandibular artery and vein. The two vessels send off medial branches that travel rostromedially with the intermandibular nerve in its final rostromedial course within the 287 mandible. The intermandibular neurovasculature makes it way to the internal opening of the intermandibular fenestra and passes through it and into the ventral oral cavity. The intramandibular vessels anastomose with the sublingual vessels and send off a dense plexus to the musk gland. The intermandibular nerve, and vessels passing with it, travels to m. intermandibularis.

Maxillary Artery The maxillary artery and vein immediately travel rostrolateral to the quadratomandibular joint capsule and curve to a rostral orientation in the sutural area between the mandibular process of the quadrate and the caudoventromedial aspect of the quadratojugal. In this area, the maxillary artery is just dorsolateral to the caudodorsolateral aspect of AME superficialis where a tendon of the muscle inserts into the dorsal and medial aspects of the surangular bone (Iordansky 1973), dorsal to the internal mandibular fenestra.

The vessels then travel rostrally across the ventromedial aspect of the quadrate toward, and then along, the ventromedial face of the quadratojugal.

Just caudal to the rostromedial aspect of the quadratojugal, the maxillary artery sends off a dorsal branch, the rostral auricular artery. The maxillary artery and vein then pass rostrally across the ventromedial face of the jugal. Throughout this rostral course, the vessels travel across the lateral aspect of AME superficialis, and send off a series of medially directed vessels into the muscle. In their course across the quadratojugal and the region of the jugal caudal to the postorbital, the vessels are positioned ventral to the lateral temporal fenestra. In the mid aspect of the lateral temporal fenestra, the maxillary artery bifurcates into dorsal and ventral branches, the facial and palatomaxillary arteries, respectively. These 288 vessels then continue their rostral course across the jugal toward the caudal aspect of the postorbital bar.

Palatomaxillary Artery Rostral to the rostral border of AME superficialis, the palatomaxillary vessels course across the lateral aspect of the rostral (=cranial ) adductor aponeurosis. A large extension of this aponeurosis forms a caudodorsally and caudolaterally directed sheet that covers the rostrodorsal and the rostrolateral aspects of AME superficialis. Further medially, the rostral adductor aponeurosis becomes confluent with the tissue of the medial aspect of the rostroventral mundplatt. The palatomaxillary vessels then pass medially across the rostrodorsal aspect of the rostral adductor aponeurosis where the tissue blankets the rostrodorsolateral aspect of AME superficialis, and then medially toward and across the area of the aponeurosis that ensheaths the rostrodorsolateral aspect of m. pseudotemporalis. The vessel then passes rostrally through the adductor aponeurosis in an area ventral to the medial face of the rostroventrolateral aspect of the ectopterygoid, which rostrodorsally forms a postorbital process that articulates with the ventromedial postorbital bone. The vessels then continue to travel rostrally, over the medial aspect of the postorbital process of the ectopterygoid.

The palatomaxillary vessels pass rostrally across the medial aspect of the sutural contact between the postorbital, which marks the rostral limit of the rostral adductor aponeurosis. The vessels then course rostral to the postorbital bar, and approach the maxillary nerve and the caudal aspect of m. pterygoideus dorsalis. 289 Facial Artery The facial artery is originally pressed against the periosteum of the caudomedial aspect of the jugal, then courses rostrally across the jugal, and travels across the ventrolateral aspect of the postorbital bar and along the medial aspect of the connective tissue of the ventral palpebra. The tendon of m. levator palpebralis dorsalis inserts along a robust process extending rostrolaterally from the rostrolateral aspect of the postorbital bar, and then runs rostrolaterally along the medial aspect of the ventral palpebra and is shortly thereafter characterized by muscle tissue. A large branch of the mandibular nerve enters into the infraorbital space through a foramen, the rostroventral postorbital foramen, in the rostroventromedial aspect of the jugal contribution to the postorbital bar. The nerve courses rostrodorsally toward and then into m. levator palpebralis dorsalis. Passing into the infraorbital space through the rostroventral postorbital foramen, with the mandibular nerve branch, is the caudal internal jugal artery which turns medially and anastomoses with the palatomaxillary artery. Just rostral to the postorbital bar, the facial artery sends off a dorsal branch that courses across the lateral aspect of the muscle tendon and then ramifies into a plexus that extends across the medial aspect of the thinner tissue characterizing the dorsal extension of the ventral palbebra. Further rostrally, the facial artery sends off a rostroventrally directed vessel that runs across the lateral aspect of the nerve to m. levator palpebralis dorsalis, and then trifurcates. (1) A caudal branch runs caudoventrally, gives off a dorsal branch to the muscle tendon, and then anastomoses with the palatomaxillary artery.

(2) A rostral branch courses rostroventrally and bifurcates along the lateral floor of the infraorbital space formed by the ventromedial extension of the jugal into a branch that runs caudally and anastomoses with the caudoventral branch of the facial artery, and a branch that courses rostrally to anastomose with the palatomaxillary artery. (3) The rostral extension of 290 facial artery courses across the medial aspect of the jugal and sends off a ventral branch which then forms a plexus with its parent vessel before anastomosing with the palatomaxillary artery. The facial artery continues to course rostrally and sends off a series of large branches that pass lateral to the tendon of m. levator palpebralis dorsalis and form a plexus in the thin dorsomedial component of the ventral palpebra, after which the facial artery courses across the lateral aspect of the nerve to the above muscle. The vessel then curves medially within the thick connective tissue, issuing from the rostroventral aspect of the ventral palpebra that forms the rostroventral periorbital fascia. Further associated with the ramifications of the facial artery is a dense plexus along the ventrolateral aspect of the postorbital bar, and another dense plexus along the caudodorsal face of the aspect of the jugal comprising the infraorbital floor.

Rostral Auricular Artery The rostral auricular artery courses rostrodorsally across the rostroventral aspect of the postorbital process of the quadratojugal, along the lateral aspect of AME superficialis, toward the ventrolateral cartilaginous border of the external auditory meatus. Upon reaching this cartilaginous border, the rostral auricular artery runs rostrally across the ventral aspect of the external auditory meatus toward the dorsolateral aspect of the postorbital bar. In the rostrodorsalmost aspect of the lateral temporal fenestra, between the postorbital bar and the external auditory meatus, the rostral auricular artery and vein break up into a plexus of large, mostly venous, anastomosing vessels that fill this aspect of the lateral temporal region. The vessels of this plexus then continue to course rostrodorsally, and upon approaching the dorsolateral aspect of the postorbital, the vessels anastomose into a plexus with the temporoorbital artery derivatives that pass through the dorsal postorbital canals. 291 Additionally, the rostral auricular artery sends off ventral branches that anastomose across

the postorbital with branches from the facial artery.

The palatomaxillary artery gives off a lateral artery, the caudal internal jugal artery,

that passes into the caudal postorbital foramen, located along the caudoventromedial aspect

of the jugal component of the postorbital process, with a branch of the mandibular nerve,

the nerve to m. levator palpebralis dorsalis. Further rostrally, the lateral branches of the

trigeminal artery join the palatomaxillary artery.

The palatomaxillary artery then sends off a series of dorsal branches that anastomose

with the facial artery, and then the palatomaxillary artery travels rostromedially across the

ventral aspect of the facial artery.

Infraorbital Space Along the rostroventromedial aspect of the postorbital process of the ectopterygoid,

the palatomaxillary artery gives off a rostrodorsal branch that trifurcates into: (1) a caudal

branch that courses dorsally to anastomose with the facial artery; (2) a dorsal branch that

courses dorsally and breaks up into a plexus along the medial aspect of the jugal; and (3) a

rostral branch that is the rostral continuation of the palatomaxillary artery. Just rostral to the

ectopterygoid, the maxillary nerve crosses over the dorsal aspect of the palatomaxillary

artery. The maxillary nerve bifurcates into a rostrodorsal branch, the dorsal alveolar nerve, that courses toward the maxilla, and a bulbous ventral branch that courses ventrally. The ventral branch of the maxillary nerve bifurcates into a rostral branch, the palatine nerve, and a caudal branch, which courses caudoventromedially with the palatopharyngeal artery through the caudal aspect of the suborbital fenestra and then across the ventral aspect of the ectopterygoid. 292 Just lateral to the bulbous region of the trigeminal nerve along the ventrolateral aspect of m. pterygoideus dorsalis and medial to the maxillary vein, the palatomaxillary artery bifurcates into rostral and ventral branches. The ventral branch courses rostroventromedially on the ventral aspect of the palatine nerve, and this gives off the palatopharyngeal artery which courses caudoventromedially along the ventral aspect of the palatopharyngeal nerve. In their paths, both the palatine and palatopharyngeal arteries give off medial vessels into m. pterygoideus dorsalis. Also in this region, the palatomaxillary artery gives off a lateral artery, the rostral internal jugal artery, that enters into the rostral jugal foramen and courses through the jugal.

In the vicinity that the palatomaxillary artery sends off its ventral branch, the palatomaxillary artery bifurcates into two dorsal branches, the dorsal alveolar and internal maxillary arteries, which essentially split across the maxillary vein. The internal maxillary artery courses rostrodorsally across the medial aspect of the maxillary vein to the vein’s dorsal aspect, and the dorsal alveolar artery courses rostroventrally across the medial aspect of the vein to the vein’s ventral aspect. All three vessels course rostrally through the infraorbital space along the dorsolateral aspect of the dorsal alveolar nerve. The internal maxillary artery courses along the dorsolateral aspect of the maxillary vein and has several anastomoses with the facial artery, as discussed above. The dorsal alveolar artery courses along the ventromedial aspect of the maxillary vein. Throughout their parallel course, the dorsal alveolar and internal maxillary arteries send off a series of vessels across the dorsal and ventral aspects of the maxillary vein that anastomose together and form an arterial plexus around the vein. 293 Along the caudoventromedial aspect of the lacrimal bone, the internal maxillary

artery, and rostrolaterally oriented branches of the maxillary vein and the dorsal alveolar

nerve, course into a caudally facing foramen, the caudal maxillary foramen, in the

caudodorsomedial aspect of the maxilla ventral to the maxilla-lacrimal sutural contact, and

then continue to course through a canal running rostrally through the maxilla (Rathke 1866;

Hochstetter 1906). The bundle then sends off neurovascular bundles that pass out the

nutrient foramina across the external aspect of the maxilla.

Just caudal to its entrance into the caudal maxillary foramen, the internal maxillary

artery sends off a large rostromedially directed vessel that courses across the dorsal aspect of

the maxillary vein and then anastomoses with the dorsal alveolar artery. Rostral to this last

anastomosis, the dorsal alveolar neurovascular bundle courses rostromedially across the

ventral aspect of the lacrimal bone, and across the rostrodorsal aspect of m. pterygoideus

dorsalis, toward the dorsal alveolar bundle. In this region along the lacrimal bone and caudal

to the dorsal alveolar canal, the dorsal alveolar artery gives off a dense array of vessels that

form a plexus with vessels from the facial artery. Also, the maxillary vein is still surrounded

by a plexus of mostly longitudinally oriented arteries, an arteriae comitantes, and these too contribute to this last plexus. The plexus extends through a thick connective tissue which is situated between m. pterygoideus dorsalis and the ventral aspect of the lacrimal bone, and which becomes confluent with the tissue of the rostroventrolateral periorbital fascia further caudomedially.

Contributions to the Palatine Artery The rostralmost continuation of the submandibular artery, the palatopharyngeal

artery, courses rostromedially across the ventral aspect of the pterygoid bone toward the 294 caudoventral aspect of the ectopterygoid bone, and runs across the pterygoid-ectopterygoid

suture. The vessel then courses rostrally across the ventromedial aspect of the

ectopterygoid, along the medial face of the lateral border of the suborbital fenestra, and

across the ventrolateral aspect of m. pterygoideus dorsalis. In longitudinal section, the

ectopterygoid is shaped as an arch, the area of the bone rostral to its postorbital process is

horizontally oriented and laterally articulates with the jugal and maxilla, whereas the area

caudal to its postorbital process is shaped as a rostrodorsal to caudoventral curve and the

caudomedial aspect of the bone articulates with the pterygoid. The palatopharyngeal artery

courses rostrodorsally to the area of the ectopterygoid medial to the bone’s postorbital

process and between the bone’s rostral and caudal components, and then travel

rostrodorsally into the infraorbital space where it anastomoses with the palatine artery. The

palatopharyngeal artery anastomoses with the palatine artery in the area where the vessel

begins to turn rostrally from its original ventral orientation, and thus, the palatine artery has the appearance of splitting into rostral and caudoventral (palatopharyngeal artery) vessels, so the true origin of the palatopharyngeal artery is not exactly clear. As the palatopharyngeal artery anastomoses with the palatine artery, the former vessel meets with a caudoventromedially oriented branch of the maxillary artery which then courses with the artery caudoventromedially across the ectopterygoid and into the pharyngeal space.

The dorsal ramus of the pterygoid artery ramifies to form a dense plexus across the

quadrate and prootic, medial to AM caudalis, which more rostrally anastomoses with vessels

from the trigeminal artery. Vascular components of this trigeminal-pterygoid arterial

network travel rostroventrolaterally through the musculature of the lateral temporal space

toward the caudal aspect of the suborbital fenestra infraorbital space. The larger vessels in 295 this network are derived from the trigeminal artery. Also, the palatine ramus of the artery of the pterygoid canal courses rostrolaterally across the dorsomedial aspect of the pterygoid toward the caudal aspect of the suborbital fenestra. Along the caudodorsolateral aspect of the palatine bone, which forms the caudal border of the suborbital fenestra, the palatine ramus anastomoses with a vessel(s) from the trigeminal-pterygoid plexus, and this (these) vessel(s) travels a short rostrolateral distance and anastomoses with the palatopharyngeal artery before this last vessel anastomoses with the palatine artery.

Palate and Palatine Artery Along the medial border of the rostrolateral aspect of the suborbital fenestra, and along the rostrolateral aspect of m. pterygoideus dorsalis, the palatine artery, vein, and nerve travel rostroventrolaterally past the suborbital fenestra to the caudoventral aspect of the maxilla. See Figure 10C for a depiction of the arterial vasculature of the palate. The neurovascular bundle then courses rostrolaterally to the ventrolateral aspect of the maxilla, and then travels rostrally across the ventral aspect of the maxilla and the dorsal aspect of the palatal mucosa. Throughout its course, the neurovascular bundle sends off dorsal branches that pass through a dense longitudinal series of foramina in the ventrolateral aspect of the maxilla and which open into the dorsal alveolar canal. Upon entering the canal, the vessels anastomose with the dorsal alveolar artery and vein. A particularly important foramen in this series is just rostromedial to the maxilla-premaxilla suture, which is the remnant of the archosaurian ventral subnarial foramen. The vessels pass through the subnarial foramen and enter into the paranasal blood space, and anastomose with the dorsal alveolar vessels. The vessels resulting from this anastomosis either continue to pass rostrally through the premaxillary aspect of the dorsal alveolar canal or pass through the medial subnarial foramen 296 in the medial premaxilla-maxilla suture and travel rostromedially to supply the narial cavernous tissue. Rostral to the ventral subnarial foramen, the palatine neurovascular bundle courses rostromedially across the rostromedial curvature of the ventrolateral premaxilla, and sends off dorsal branches through a continuing series of foramina which open into the premaxillary component of the dorsal alveolar canal. The rostromedialmost foramina are large and open directly into the rostroventral aspect of the nasal vestibule. The vessels that pass dorsally through these last foramina then travel caudally to supply the narial cavernous tissue.

Throughout its course, the palatine artery sends off a dense series of lateral vessels that travel laterally across the bony palate and anastomose with one another, and with medial branches from the opposite palatine artery, to form a dense plexus that covers the entire bony palate and the palatal mucosa. Vessels derived from the medial branches of the submandibular artery, and that supply and ramify through the choanal torus, course rostrolaterally across the ventral aspect of the pterygoid and then the palatine. These vessels form a plexus across the ventral aspect of the palatine, and then send off a plexus of rostromedially oriented vessels that anastomose with the palatine artery along the caudoventral palatal process of the maxilla as the palatine artery passes to this aspect of the maxilla from the suborbital fenestra. However, unlike neornithines, the anastomotic relationship between the palatine artery and elements of the submandibular artery does not appear to form a single median palatine artery that courses rostrally across the palate.

Oromandibular Trunk Proximal in its rostroventral course, the oromandibular trunk sends off a dorsolaterally directed branch that courses across the caudodorsal aspect of m. pterygoideus 297 ventralis to the caudodorsal aspect of m. depressor mandibulae, and then ramifies across and

within this aspect of the muscle. The oromandibular trunk then courses

rostroventromedially across the medial aspect of m. pterygoideus ventralis toward the

tendon of m. rectus capitis dorsalis. After reaching the tendon, the vessel courses

caudoventrally across the lateral aspect of the tendon, and across the medial aspect of m.

pterygoideus ventralis to the dorsolateral aspect of m. rectus capitis ventralis pars lateralis

(henceforth RCVL). After exiting into the occipital region through the external glossopharyngeal foramen, the glossopharyngeal nerve courses caudoventrally across the lateral aspect of the tendon, and courses across the medial aspect of the oromandibular trunk, after which the nerve passes to the caudal aspect of the vessel, and then continues its course by following along the caudal aspect of the artery.

At the dorsolateralmost aspect of RCVL, the oromandibular trunk sends off a vessel

that travels a short, rostral distance to anastomose with the internal carotid artery. The

oromandibular trunk and glossopharyngeal nerve then travel caudoventrally across the lateral

aspect of RCVL. The vagus nerve exits into the cervical region from the external vagus

foramen, dorsal to RCVL, and medial to CN IX, and then travels caudoventrally across the

medial and to the caudal aspects of CN IX, and then meets with the caudal cephalic +

temporomandibular vein. Subsequently, CN X travels caudoventrally across the lateral

aspect of RCVL and then turns to travel along the lateral aspect of the caudal cephalic +

temporomandibular vein. The hypoglossal nerve travels rostroventrally across the lateral

aspect of these various neurovascular structures near their intersection along RCVL. After

receiving the stapedial vein, the caudal cephalic + temporomandibular vein courses

caudoventrally across the rostrolateral aspect of the tendon of m. rectus capitis lateralis. At 298 the rostroventrolateralmost aspect of the tendon, the oromandibular vein drains into the caudal cephalic + temporomandibular vein and forms the jugular vein.

Upon reaching the ventrolateral aspect of RCVL, the oromandibular trunk sends off a series of vessels to the thyroid gland, and CNs IX and X send off fibers to one another across the lateral aspect of the trunk. The oromandibular trunk then divides into rostral and caudal branches. The rostral branch travels rostrolaterally with a branch of CN IX to the hyoid.

The caudal branch of the oromandibular trunk bifurcates into rostral and caudal rami, at the ventromedial aspect of m. pterygoideus ventralis and positioned between the ventrolateral aspect of RCVL and the dorsolateral aspect of m. RCVM. The rostral ramus travels rostrolaterally with a branch of CN IX, to the esophagus. The caudal ramus, the vagus artery, courses caudally with CN X and the jugular vein as a neurovascular bundle across the dorsolateral aspect of RCVL and the ventrolateral aspect of m. rectus capitis dorsalis.

Buccopharyngeal Cavity

Surface Anatomy of the Region of the Choanae and Rostrodorsal Pharynx The epithelium of the lateral pharyngotympanic tube travels through a cartilaginous tube. The cartilaginous tube is medially continuous with a cartilaginous-like tissue that surrounds a darkly pigmented bulbous structure protruding from the median pharyngeal foramen. The cartilage does not cover the black bulb. The cartilaginous-like tissue that surrounds the bulb’s rostral aspect continues rostrally and forms a disk-like structure that fills the deep fossa located between the median pharyngeal foramen and the choanae. 299 Additionally, this white cartilaginous-like tissue tapers into a triangular structure with

the apex pointing laterally. The tissue has a rostral component near its triangular apex that

travels toward the epithelial tissue of the lateral pharyngotympanic tube, after which the

cartilaginous-like tissue becomes softer and passes into the lateral pharyngotympanic fissure as a cartilaginous capsule. The capsule passes through the fissure as a thin rod that surrounds the lateral pharyngotympanic epithelial tissue. Before passing into the fissure, a portion of the cartilaginous-like tissue comprising this rod extends caudolaterally along the

ventral aspect of the basal tubercle and to a position just rostral to the internal carotid artery

foramen, and extends caudally to the rostral border of this foramen.

Deep to this extensive cartilaginous-like tissue system is a sac of darkly pigmented

tissue. This pigmented tissue is an extension of the tissue protruding from the median

pharyngeal foramen which forms the center of this tissue complex. This dark tissue spans

out rostrally from the bulb forming the median pharyngeal sac, and travels across the dorsal

surface of the cartilage-like tissue overlying the space between the median pharyngeal

foramen and the choanae, and is directly continuous with the tissue of the rostral pharynx.

The cartilage-like tissue just caudal to the median pharyngeal bulb, along with the tissue

extending from the bulb, is continuous with large, lateral, and extensively rippled sac-like

projections of the pharynx. The tissue forming these projections has an appearance similar

to the smoother pharyngeal wall.

Pharyngeal branches from the palatopharyngeal artery travel to and across the ventral

aspect of the mucosa covering the ectopterygoid which they extensively supply. The

pharyngeal vessels then travel ventromedially to the region adjacent to the median

pharyngeal sac and send off vessels that supply the sac. The pharyngeal vessels send off 300 rostral branches to the fossa caudal to the choanae which ramify in this area and give off branches to the tissue of the choanae and to the thick choanal torus which closes off the choana. The pharyngeal plexus surrounding the median pharyngeal pouch travels laterally to ramify across the epithelium of the lateral pharyngotympanic tube. Additionally, these pharyngeal vessels send off caudolateral branches to the rippled, lateral pharyngeal sacs.

These lateral pharyngeal sacs are just deep to the common carotid artery which sends off arteries that travel ventrally into the sac and contributes to the plexus within the sacs. The lateral pharyngeal sacs are further supplied from elements of a highly vascular region of the pharynx just caudal to the median pharyngeal bulb. The multiple sources of supply to the plexus within the tissue forming the pharyngeal sacs create a dense, perhaps erectile, vascular tissue, characterized by arteriovenous anastomoses. The large, paired, thymus glands are dorsal and caudal to the lateral pharyngeal sacs, and are supplied by vessels from the sacs which form a dense vascular plexus supplying and draining the gland. The plexus within the thymus gland possesses arteriovenous anastomoses.

The tissue that gives rise to the thick choanal torus is extremely vascular, and attaches to the caudoventral aspect of the pterygoid; it passes medially across the caudoventromedial surface of the pterygoid and inserts dorsolaterally along the basal tubera in a position rostroventral to the lateral pharyngotympanic fissure. Rostrally the tissue of the choanal torus becomes much thicker and densely vascular, and forms a rostromedial to caudolateral curved flap on the lateral aspect of the choanae.

Taken together, the area extending from the choanae to the rostral pharynx presents a complex vascular network, with some particularly vascular tissues (choanal torus), and potentially erectile tissues (the lateral pharyngeal sacs). However, because of the extensive 301 cartilage-like tissue covering, much of this area is not directly in contact with the air-stream.

The choanal torus, the median pharyngeal protuberance, and the lateral pharyngeal sacs would have the most exposure to air in this region.

Mucosa and Relationships of the Laryngophayrnx The ostium and diverticula of the median pharyngeal tube, and the opening of the choanae and the choanal torus are situated in the dorsal aspect of the laryngopharynx, and the basihyale and mons layrngis are situated in the floor of the laryngopharynx. The floor and roof of the laryngopharynx are laterally connected by a wall of rugose pharyngeal mucosa. The rostral aspect of the basihyale expands dorsally and slightly rostrally to form a wide wall separating the oral cavity from the laryngopharynx.

The cavum pharyngis is a longitudinally oriented fossa along the basihyale situated between the laryngeal cartilages and the lateral laryngopharyngeal wall. The basihyale cartilage and the cavum pharyngis is covered by a pharyngeal mucous membrane with caudodorsally oriented rugae across the cavum pharyngis which become rostromedially oriented across the rostrodorsal aspect of the basihyale. The mucosa across the rostrodorsal basihyale is thick and light in color. The rostralmost aspect of the pharyngeal mucosa along the basihyale spreads rostroventrally across the rostral face of the cartilage, and then bends rostrally to become confluent with the caudodorsal aspect of the tongue. The caudodorsal tongue is characterized by a thick, light colored mucosa with longitudinal rugae that are continued from the rugae of the laryngopharyngeal mucosa, and more rostrally the tongue is characterized by a darker tissue covered by taste buds. The caudalmost area between the laryngopharyngeal tissue and the tongue is characterized by a deep mucosal recess. 302 The caudal aspect of the mucosa of the cavum pharyngis is continuous with the

mucosa of the rostral esophageal floor. M. hyoglossus pars medialis originates from the

caudodorsalmost aspect of the basihyale and runs rostrally to comprise most of the muscular

tongue, whereas pars medialis originates from the caudolateral surface of the basihyale and

runs along the ventrolateral aspect of pars medialis (Schumacher 1973). The latter muscle

becomes associated with the genioglossal musculature through a raphe in their rostral course

across the ventral and ventrolateral tongue. The lateral aspect of the basihyale protrudes the

mucosa of the laryngopharyngeal wall, bordering the lateral cavum pharyngis medially. Just

dorsal to this fold is a fold of thicker mucosa formed mainly by the medial bulge of m.

hyoglossus medialis that continues to cross rostromedially to become continuous with the

thick mucosa of the rostrodorsolateral basihyale. A caudolateral continuation of this last fold

bends ventrally and then curves rostrally across the ectopterygoid bone to become

continuous with the caudal aspect of the thick torus mucosa of the choanal ridges. The

caudal continuation of the fold is confluent with the mucosa of the medial floor of the

esophagus.

Hyolingual Artery The hyolingual artery courses rostromedially across the ventral aspect of m.

pterygoideus ventralis from the median to medial aspect of the muscle. The vessel continues

its course, traveling across the ventromedial m. pterygoideus ventralis along the lateral aspect of the caudal belly of m. sternohyoideous pars lateralis and ventral to the medial aspect of m.

constrictor colli. See Figure 12 for a diagram of the divisions of the hyobranchial

musculature and for comparisons with birds. In this region, m. sternohyoideous pars

medialis rests against the trachea and is rostrally positioned across the ventrolateral basihyale. 303 The m. coracohyoideous muscle body rests just lateral to m. sternohyoideous pars medialis and has a tendon that inserts along the caudoventrolateral ceratobranchial (Schumacher

1973). M. sternohyoideous pars lateralis rests just ventral to the area where the former two muscles meet In this area, the lingual artery gives off a large branch that courses medially across and supplies the dorsal aspect of m. constrictor colli and the ventral aspect of m. sternohyoideous pars lateralis, further medially, m. coracohyoideous, and dorsomedially, the ventral aspect of m. genioglossus medialis where it inserts into and is positioned against the central ventral hyoid.

The hyolingual artery continues to travel rostrally, to an area ventrolateral to m. branchiomandibularis visceralis and dorsolateral to m. sternohyoideous pars lateralis. In this area the vessel bifurcates into medial and rostral vessels. The medial vessel, the laryngeal artery, is discussed in the section on the laryngopharynx vasculature. The rostral artery, the lingual artery curves lateral to m. sternohyoideous pars lateralis and medial to m. pterygoideus ventralis toward the caudolateral aspect of m. hyoglossus. The vessel sends off a smaller branch that passes medially, then caudomedially between m. sternohyoideous pars lateralis and m. contrictor colli, and then finally across the ventral belly of the latter muscle.

The lingual artery then courses rostrodorsally across the ventromedial surface of m. branchiomandibularis visceralis, the ventrolateral aspect of m. sternohyoideous pars lateralis, and the caudolateral aspect of m. hyoglossus. The artery then bifurcates into dorsal and ventral vessels, the proper lingual and sublingual arteries, respectively. The sublingual artery travels ventrolaterally across the rostroventral aspect of m. branchiomandibularis visceralis and caudolateral to m. sternohyoideous pars lateralis. Ventrally, the vessel splits between the caudomedial aspect of m. intramandibularis and the rostromedial aspect of m. constrictor 304 colli. In this area the artery gives off a series of vessels to the highly vascular musk gland.

The black, highly vascular musk gland rests and spans across the area ventromedial to the caudal intermandibular foramen ventral to the medial aspect of m. intramandibularis near the region where the muscle dorsomedially inserts into the dorsal splenial bone. Ramus intramandibularis of the mandibular nerve and branches of the intramandibular arteries and veins enter the oral cavity through the caudal intermandibular foramen, dorsal to the musk gland, and the vessels supply and drain the gland. These vessels anastomose with the sublingual artery and vein. More caudally, the ventrolateral artery anastomoses with rostroventrally oriented branches of the mandibular artery that pass through the internal mandibular fenestra. The sublingual artery then courses rostrally between the dermis of the ventral oral cavity and the intramandibular muscle. Rostral to m. intramandibularis, the artery courses between the ventral aspect of m. genioglossus lateralis and the dermis to the rostral aspect of the mouth, and sends off a series of vessels that supply the dermis and ventral tongue musculature.

The proper lingual artery courses dorsomedially over the rostrodorsal surface of m. branchiomandibularis visceralis lateral to m. hyoglossus where the muscle attaches to the rostrolateral hyoid process. Just rostral to m. branchiomandibularis visceralis, the proper lingual artery anastomoses with laterally oriented branches of the mandibular artery that pass through the dorsal aspect of the caudal intermandibular foramen. Before anastomosing with the proper lingual artery, the mandibular vessels send off branches to m. sternohyoideous pars lateralis and to the dorsolateral aspect of m. branchiomandibularis spinalis. The proper lingual artery then continues to course rostromedially along the lateral aspect of m. hyoglossus lateralis and across the ventral aspect of first m. sternohyoideous pars lateralis 305 and then m. branchiomandibularis spinalis. In this course, the proper lingual artery sends off vessels that supply mm. genioglossus lateralis and hyoglossus. M. genioglossus lateralis attaches to the mid-ventral hyoid process dorsal to m. branchiomandibularis, and is more rostrally oriented across the ventrolateral hyoid. Just past the rostrolateral aspect of m. branchiomandibularis spinalis, the proper lingual artery bifurcates near the bifurcation of m. hyoglossus into lateral and medial components in an area parallel to the coronoid bone and the rostral aspect of the basihyale. The medial and lateral branches of the proper lingual artery are the medial and lateral glossal arteries, respectively.

The medial glossal artery travels rostromedially across the ventral aspect of m. hyoglossus medialis toward the lateral aspect of m. genioglossus lateralis. The vessel then travels throughout its rostral course across m. hyoglossus, dorsal to the dorsolateralmost aspect of m. genioglossus lateralis into which it sends ventral branches. Similarly, the vessel sends numerous lateral and dorsal branches to m. hyoglossus medialis.

The lateral glossal artery passes rostrolaterally along the lateral aspect of m. branchiomandibularis. The vessel then travels rostrally between m. hyoglossus lateralis and m. intramandibularis, then travels rostrally through the intramandibularis muscle and then m. genioglossus lateralis for the duration of its course.

Laryngeal Artery As mentioned above, most of the dorsal surface of the basihyale is covered by a thick pharyngeal mucosa, with tightly packed longitudinally oriented ridges that run across the tissue. The rostral and lateral aspects of the basihyale curve dorsally like the sides of a bowl. Along the curvature of the rostral basihyale, the longitudinal ridges curve rostromedially toward the midline, and at the midline the ridges curve caudolaterally to run 306 longitudinally across the other side of the basihyale. The dorsalmost aspects of the dorsal and lateral basihyale are lined by a thick, strong connective tissue very different from the pharyngeal mucosa.

The laryngeal cartilages are connected to the center of the basihyale, and partially form the epiglottis, which opens into a large cavity, the cavum pharyngis. The cavum pharyngis is formed of the cricoid cartilage, the laryngeal musculature, and connective tissues which are associated with the cricoid and arytenoid cartilages. The floor and inner walls of the mons laryngis is formed by the cricoid cartilage, whereas the outer component of the rostral mons laryngis, and the area between the caudal cricoid and the arytenoid cartilages, is formed by musculature. The mons laryngis is covered by a tough, white connective tissue that lacks ridges. The thick longitudinally oriented m. constrictor laryngis, which is lateral to the trachea, more rostrally attaches to the ventromedial aspect of the long arytenoid process.

M. dilator laryngis, a thinner more strap-like muscle, lies lateral to the cricoid cartilage, laterally covers m. constrictor laryngis, and dorsally covers m. dilator laryngis to attach along the dorsolateral arytenoid cartilage (Schumacher 1973). Together, the two muscles bulge laterally from the arytenoid process, and are dorsolaterally covered by pharyngeal mucosa, and with the arytenoid cartilage, are dorsomedially covered by mucosa from the mons laryngis. Rostral to the rostral arytenoid and the musculature that bulges caudally from it, the solid caudal mons laryngis is formed of an extremely thick, white, connective tissue similar to the thinner tissue of the mons laryngis. The tissue of the rostral aspect of the mons laryngis is filled with a dense vascular plexus. The rostral aspect of the mons larygnis is a semi-sphere shaped structure that is connected to the rostral aspect of the arytenoid process, and is connected to the rostral mons laryngis of the other side along its thin, 307 tapered, rostralmost aspect. This rostralmost component of the mons laryngis is connected

by a thick strand of connective tissue to the rostral basihyale. In sagittal section, the medial

surface of the mons laryngis is a flat wall covered by thick mucosa, and separated from the

wall of the contralateral mons laryngis by a small space.

The caudal aspect of the mucosa covered arytenoid cartilage, in section, forms a

deep, open half-circle with its concave end facing rostrally. Caudal to the arytenoid cartilage

is a wide open space, the cavum laryngis, between the cartilage and the rostralmost tracheal

ring, and the cricoid cartilage comprises the far lateral wall of the bulbous antrum.

A curved, caudodorsal to rostroventral, cartilaginous ridge that protrudes medially from the cricoid cartilage into the cavum laryngis divides the cavum into caudoventral and rostrodorsal fossae. This medial ridge is rostroventrally continuous with the rostral aspect of a median, longitudinal, cartilaginous ridge, the crista ventralis, along the floor of the cricoid that divides the antrum into two sides. The caudoventral fossa is formed by a concavity in the cricoid cartilage, rostral to the border formed by the medial process of the basihyale and caudal to the first tracheal ring. The caudoventral fossa is covered by a thin, densely vascular lining that is continuous with the densely vascular rostral trachea. The rostrodorsal fossa is a deep cul-de-sac formed by a fossa in the caudal cricoid rostrolaterally, the laryngeal muscles caudolaterally, the thick vascular connective tissue of the mons laryngis caudally and caudomedially, and the arytenoid rostromedially. The medial component of this fossa does not extend as far caudal as the lateral aspect. The cricoid cartilage of the rostrodorsal fossa is covered by the thin, vascular, inner tracheal tissue, whereas the rest of the fossa is lined by the thicker tissue of the mons laryngis. The floor of the antrum is lined by the thin and vascular tissue and continues across the floor of the trachea. 308 Between the lateral walls of the trachea and the laryngeal cartilages, there is a pharyngeal mucosa lined recess. The ventral and lateral pharyngeal walls formed by the basihyale mucosa are caudally continuous with the ventral and lateral walls of the esophagus.

The tough dorsal lining of the rostral basihyale covers and spreads ventrally across the rostrodorsal aspect of the basihyale, and is then rostrally continuous with the connective tissue that anchors the caudodorsal tongue to the basihyale. As mentioned above, between the rostral aspect of the basihyale and the caudodorsal tongue is a mucosal, horizontally oriented sulcus— except along the rostrolateralmost basihyale where the tough connective tissue forms a rostrally oriented ridge that connects to the tissue along the caudolateral process of the tongue. Laterally, this ridge is connected to the rostral aspect of the connective tissue that forms the corner of the mouth, the tissue covering the medial aspect of the mandible, and the floor between the corner of the mouth, the mandible, and the tongue. Rostrally, the tissue along the dorsal aspect of the lateral walls of the basihyale is connected to the caudal aspect of the tissue comprising the corner of the mouth and more caudally with the connective tissue covering the jaw musculature. The connective tissue of the corner of the mouth actually covers the rostral aspect of m. pterygoideus ventralis and connects to the cranial aponeurosis. Dorsally, the corner of the mouth tissue begins to forms the thick ridges along the caudal aspect of the choana. Caudal to this, the tissue along the dorsal basihyale continues dorsally to form the roof of the pharynx, and the tissue along the caudodorsal basihyale is continuous with the tissue that forms the pharyngeal diverticula.

The infundibulum of the caudal choana is found in the dorsal oropharynx dorsal to the glottis. The laryngeal artery is largely responsible for the blood supply to this complicated anatomy of the oropharynx. 309 The laryngeal artery, after branching from the hyolingual artery, passes

rostrodorsolaterally across the ventromedial surface of m. pterygoideus ventralis, medial to the ceratobranchiale, and sends off a dorsally oriented trunk that gives off caudolateral branches to m. pterygoideus ventralis and rostral branches into m. branchiomandibularis visceralis. The laryngeal artery continues across m. pterygoideus ventralis and travels dorsolaterally over m. branchiomandibularis visceralis, which it supplies. M. branchiomandibularis visceralis inserts on the angular bone, ventral to the foramen mandibulae (Schumacher 1973). At this point, the artery anastomoses with branches of the mandibular artery that pass toward the vessel from the internal mandibular fenestra. The vessel then passes medially across the dorsal aspect of m. branchiomandibularis visceralis and then across the dorsal aspect of m. sternohyoideous pars medialis which lies just lateral to the ceratobranchiale, after which the lingual artery curves rostromedially and passes across the dorsal aspect of the ceratobranchiale. The artery travels medially through the submucosa

covering the dorsolateral basihyale and sends off a vessel(s) that ultimately ramifies across

and supplies the dorsal trachea and the mucosal tissues associated with it. The artery then

curves rostrolaterally, appearing as a semicircular vessel, toward the dorsomedial

ceratobranchiale. Lateral vessels that branch from this arc supply the lateral walls of the

pharynx and more caudally of the esophagus, and ramify to anastomose with vessels within

the roof of the pharynx and esophagus, and also partially feed the vascular tissue within the

pharyngeal diverticula. An array of vessels branch from the medial aspect of the artery as it

curves. Many of these vessels ramify throughout the basihyale submucosa, and several of

the smaller branches make their way toward the rostral trachea and the floor of the 310 esophagus and pharynx. A large vessel branches medially from the middle of the arc, travels

medially toward the larynx, and sends off branches to the pharynx and trachea in its course.

A large rostral branch of the laryngeal artery, the proper laryngeal artery, courses rostrally across the lateral aspect of the larynx supplying the mucosa, and more rostrally sending vessels into the laryngeal musculature. The vessel rostromedially curves along the caudal aspect of the mons laryngis and sends vessels into the thick tissue that then ramify into the dense vascular plexus within it. The proper laryngeal artery further supplies the tissue along the median aspect of the rostrodorsal basihyale. Vessels from the rostromedial aspect of this artery travel caudally through the caudal surface of the mon laryngis, anastomose into the plexus, and send off branches that enter into, ramify across, and supply cavum laryngis, the floor of the cavum, and the rostral trachea. Corrosion casts of the mons laryngis demonstrate two parallel, densely vascular, cavernous tissue-like tunnels that open into the trachea. A large rostral branch and smaller rostral branches from the laryngeal artery arc travel dorsally along the corner of mouth, and ultimately course to the plexus within the lateral choanal torus and the caudal choana. The rostromedial continuation of the laryngeal artery near the rostromedialmost aspect of the ceratobranchiale travels ventrolaterally under the process and just lateral to the process anastomoses with the lingual artery.

Nasal Cavity

Olfactory Tract and Vasculature In their rostral course toward the nasal cavity, the olfactory tract and associated

vasculature run through a longitudinal cartilaginous canal formed of the supraseptal cartilage 311 and resting upon the orbital septum. The supraseptal cartilage appears to be an outgrowth of an expanse of cartilage derived from the dorsolateral orbital septum.

As the olfactory tracts expands rostrally into the olfactory bulbs and the supraseptal cartilage expands to accommodate it. On the lateral aspect of the rostral supraseptal cartilage is a second cartilaginous canal that parallels the course of the olfactory tract. The medial wall of this second cartilaginous canal apparently serves as the medial wall of the olfactory canal. In the middle of the rostralmost aspect of the olfactory bulb cartilage, facing caudally into the olfactory bulb vestibule, is a triangular protuberance that begins dorsolaterally and tapers toward a point ventrally. The ventral apex is continued by a median, longitudinal, caudally running ridge of cartilage that only slightly divides the ventral aspect of the olfactory bulb vestibule.

A rostral extension of the meningeal sleeve that surrounds the olfactory tracts, commonly ensheathes the olfactory bulbs. The two ethmoidal arteries run rostrally closely apposed to one another along the ventral aspect of the meninges covering the olfactory tract and bulb, and between the dorsal aspect of the olfactory tracts.

Near the rostral end of the vestibule, the olfactory bulb begins to break up into a series of large nerves that pass out of the vestibule. For instance, in a specimen of Alligator, in the vestibule floor lateral to the area where the median ridge expands dorsally, there is a large oval opening for the exit of a large nerve. Lateral to this opening is a smaller opening, and again lateral to this is a third, larger opening. Rostroventrally oriented nerves pass out of the floor of the vestibule. Dorsal and lateral to the lateral opening in the floor, along the lateral wall of the vestibule, is a large ventrolateral opening and another smaller one dorsal to this. Rostrolaterally directed nerves pass through these lateral foramina. Lateral to the 312 dorsal aspect of the now widened median ridge is a small opening, dorsolateral to this is a

second opening, and ventrolateral to this second opening, is a final opening. Rostrodorsal

nerves pass through these dorsal openings.

Along the rostroventralmost aspect of the olfactory bulb, the ethmoidal artery and

vein ramify to form a vascular plexus spread across the rostral aspect of the olfactory bulb

and against the corresponding cartilage of the olfactory vestibule. In all injected specimens,

the venous network within the vascular plexus appears sinus-like.

Just caudal and lateral to the caudalmost aspect of the median ridge, the ethmoidal

artery and vein send off branches that curve dorsolaterally, and then pass laterally through an

opening in the caudolateral wall of the olfactory vestibule. These vessels then pass into the

orbitonasal canal lateral to the olfactory vestibule. Within the orbitonasal canal, the

ethmoidal vessels immediately anastomose with the supraorbital + ophthalmotemporal

vessels and form the nasal artery and vein. The profundus nerve and the nasal vessels then

travel rostrally through the orbitonasal canal and at the rostral aspect of the canal, medial to

the rostral aspect of the prefrontal, divide into the medial and lateral nasal neurovasculature

(Witmer 1995b). The medial neurovasculature travels ventromedially, exits the canal, and

enters the caudodorsomedial aspect of the nasal cavity through an opening in the

ventromedial surface of the cartilaginous canal, the fenestra adhevens. The lateral nasal neurovasculature travels rostrally out of the canal and onto the caudodorsal surface of the nasal cartilages through the foramen epiphanale (Witmer 1995b). See Figure 10A-B for a depiction of the course of the medial and lateral nasal arteries in the nasal cavity. 313 Medial Nasal Artery The medial nasal artery and nerve travel rostrally across the dorsal aspect of the nasal septum (Witmer 1995b), and the vessel immediately sends off a ventral branch, the postconchal artery, that travels rostroventrally to the caudodorsal aspect of the postconcha and then bifurcates into medial and lateral branches. The medial branch travels and ramifies across the medial aspects of the concha, whereas the lateral branch ramifies across the lateral surfaces of the concha.

After sending off the postconchal artery, the medial nasal artery travels rostrally near the dorsomedial aspect of the concha and sends off a ventral branch, the conchal artery.

The conchal artery courses rostroventrally across the caudodorsal aspect of the cavum concha and then bifurcates into medial and lateral branches that supply the medial and lateral aspects of the concha, respectively. Rostrally, the medial nasal artery gives off a series of branches that travel laterally across the concha

The medial nasal vasculature then travels rostroventrally near the medial surface of the roof of the pre-concha. In their path, the nerve and artery send off branches that ramify across the preconcha. The artery and nerve then travel rostroventrally across the medial aspect of the nasal septum. Ventrally, the tissue of the internasal septum is confluent with the solum nasi, and, in a region caudal to the transverse plane of the premaxilla-maxilla suture, the medial nasal artery reaches the solum nasi. The vessel then ramifies through the solum nasi, sending off vessels that anastomose with branches of the “sphenomaxillary” and dorsal alveolar arteries. Together these vessels form a dense plexus in the rostral submucosa of the solum nasi, extending caudally from the area of the medial subnarial foramen and to the rostral aspect of the nasal vestibule. The plexus is especially dense in the nasal vestibule, 314 and rostrally receives additional blood from ramifying vessels derived from the premaxillary

arteries.

Lateral Nasal Artery and Vein The lateral nasal nerve, vein, and artery enter the nasal cavity through the foramen

epiphanale dorsal to the tectum nasi, ventral to the nasal bone, and in the vertical plane

where the caudodorsal root of the cavum concha originates from the tectum nasi (Witmer

1995b). The neurovasculature then travels rostrally through a sleeve that inserts into the

nasal bone between the postconcha and cavum conchae, and then becomes unbound from

this sleeve and travels across the dorsolateral aspect of the region of the tectum nasi that

forms the roof of the concha. The vessel then travels through a sleeve between the cavum

conchae and the preconcha, and further rostrally, the vessels travel across the region of the

tectum nasi that forms the roof of the pre-concha.

In its course, the lateral nasal artery travels lateral to the lateral nasal nerve and

through the nasal gland, which runs longitudinally across the ventral aspect of the nasal-

maxilla sutural contact (Witmer 1995b). The lateral nasal vessels sends off an array of

vessels that ramify through, and form a dense plexus within the nasal gland (Witmer 1995b)

In its proximal course, the lateral nasal vein travels along the medial surface of the lateral nasal artery. The lateral nasal vein then bifurcates into lateral and medial branches.

The bifurcation occurs in the transverse plane of the rostral lacrimal-maxilla suture, and the caudal aspect of the caviconchal recess. The lateral branch continues to travel on the medial aspect of the lateral nasal artery, whereas the medial branch travels along the ventral surface of the artery. 315 Medially, the wide nasolacrimal gland rests against the lateral surface of the lateral nasal artery and the lateral branch of the lateral nasal vein, and laterally the gland rests within a deep fossa in the medial aspect of the maxilla (Witmer 1995b). This lateral face of this aspect of the medial maxilla forms the medial border of the caviconchal recess. The gland is wrapped in a sac of thick black tissue. This gland was found to be extremely vascular through gross dissection and corrosion casts (in fact, the plexus of the nasolacrimal gland appears to be far denser than the plexus of the nasal gland). A dense vascular plexus, derived from branches of the supraorbital, ophthalmotemporal, facial, and dorsal alveolar vessels, spreads and ramifies throughout the gland. The lateral nasal artery sends off a series of vessels that travel laterally to, and ramify within, the nasolacrimal gland plexus. Similarly, the ventral branch of the lateral nasal vein receives a series of tributaries that drain medially from the gland.

Approaching the rostroventral surface of the nasal bone, the lateral nasal vessels begin to ramify into a complex vascular network ultimately associated with the blood supply to the narial erectile tissue. The lateral nasal artery bifurcates into two long and large vessels, the lateral and medial erectile arteries, respectively. The medial erectile artery travels rostromedially, across the dorsal aspect of the lateral erectile vein. The artery then continues to course toward the medial aspect of the narial erectile tissue, and runs along the medial aspect of the medial erectile vein and the lateral aspect of a branch of the lateral erectile vein that also travels to the medial erectile tissue. These vessels course ventral to the rostral narial process of the nasal bone. Upon reaching the medial aspect of the narial cavernous tissue, the artery ramifies and anastomoses with vessels within the cavernous network. In some specimens, the medial erectile artery is not a well defined single vessel, but rather the artery is 316 represented by a series of small arteries that travel together to the medial erectile mass and follow the path described above.

The lateral erectile artery travels rostrolaterally along the ventrolateral surface of the lateral branch of the lateral nasal vein toward and then through the rostrolateralmost aspect of the nasal gland just caudal to the area where the glandular tissue blends into the caudomedialmost aspect of the constrictor muscle of the nostril (as illustrated in Bellairs and

Shute 1953). Within this tissue intersection, the lateral erectile artery bifurcates into medial and lateral branches. The rostral branch travels rostrally through the narial constrictor muscle and then travels through the dilator muscle of the nostril. Finally, the rostral branch travels rostrally into the caudolateral tissue of the cavernous mass, and ramifies into vessels that contribute to the erectile vascular network. The lateral branch of the lateral erectile artery travels through the glandular tissue toward the medial subnarial foramen and anastomoses with the medial subnarial artery. As a result of this anastomosis, the medial branch of the lateral erectile artery carries blood to the narial erectile tissue derived from both the lateral nasal and the dorsal alveolar arteries.

The lateral branch of the lateral nasal vein travels along the ventromedial aspect of the medial erectile vein to the medial subnarial foramen and anastomoses with the medial subnarial vein. Caudomedial to this anastomosis, the lateral branch of the lateral nasal vein sends off a medial branch that travels rostrolaterally and anastomoses with the rostral erectile vein.

The rostral branches of the lateral nasal + medial subnarial anastomosis, the cavernous artery and vein, course along the medial aspect of the premaxilla and through a cavernous-appearing tissue that is spread along the lateral surface of the nasal cupola. Along 317 the caudolateral aspect of the nasal cupola, the cavernous artery and vein send off medial

branches that pierce the cupola and enter to the caudoventral region (the “tail”) of the narial

erectile mass. These vessels then course medially through the tissue and send off a series of

vessels that greatly contribute to the erectile tissue. The cavernous vessels then continue to

course across the nasal cupola and along its rostrolateral surface, and the cavernous vein

turns medially to pierce and pass through the cupola and enter the rostroventral main mass

of the erectile tissue. This rostral cavernous vein travels medially through the tissue and

sends of a considerable number of veins into the vascular network. When sectioned para-

sagittally, the two cavernous veins present prominent, wide bores and clearly stand out

amongst the spongy array of the other vessels.

Just rostromedial to the bifurcation of the lateral nasal artery, the lateral nasal vein

bifurcates into the medial and lateral erectile veins. The large medial erectile vein travels rostromedially across the nasal bone and toward the ventral aspect of the sutural contact between the two nasal bones. In this course, the medial erectile vein sends off large size vessels that course rostromedially and anastomose with similar vessels from the contralateral medial erectile vein. Additionally, these last veins ramify into large torturous veins that form a loose venous plexus against the roof of the nasal cavity along the median rostral aspect of the nasal bones, and just caudal to the nasal vestibule. The two medial erectile veins ultimately anastomose together and form a single large vessel that travels into the median caudal component of the narial erectile mass. Caudal to the erectile mass, the joined medial erectile vein continues to contribute to the plexus along the nasal cavity roof.

The lateral erectile vein travels rostrally across and then past the ventral surface of

the medial erectile artery, and then bifurcates into medial and lateral branches, the narial and 318 rostral erectile veins, respectively. The rostral erectile vein travels rostrally through the constrictor muscle of the nostril, then the dilator muscle of the nostril, and ultimately makes its way into the narial erectile tissue.

The narial vein travels rostromedially through the constrictor muscle of the nostril

into the area dorsomedial to the nostril, and sends off a medial branch that anastomoses

with its contralateral counterpart, and connects the two narial muscle-narial erectile tissue

masses. The continuation of the medial narial vein courses rostrally across, and contributes

to the vasculature of, the medial area of the nostril. Further rostrally, the vein curves

medially through the rostromedial tissue of the nostril and then travels through the rostral

tissue of the nostril and ramifies into a plexus of large caliber veins that spreads throughout

the tissue of the rostral border of the nostril and the narial cavernous tissue.

Narial Erectile Tissue and the Nostril Lateral and medial to the narial canal, the tissues of the erectile mass and the narial

musculature become continuous, and the vascular networks within both areas freely

anastomose and interconnect. It is also important to note that the submucosa and nasal

glandular tissue dorsal to the tectum nasi, especially rostrally, is particularly vascular and

contains complex anastomotic relationships. In fact, in section this tectal tissue is quite

spongy and definitely gives the appearance of an erectile tissue. Rostrally, this tissue

continues into the tissue system associated with the narial musculature.

Similarly, the submucosa of the solum nasi becomes increasingly vascular as it

spreads rostrally through the nasal cavity, and is especially vascular within the nasal vestibule

where if forms the vestibular floor. Rostrally, the solum nasi is continuous with the

cartilaginous tissue that lines the rostral aspect of the nasal vestibule which is formed by the 319 premaxilla. Dorsally this last tissue becomes confluent with the rostrodorsal aspect of the nasal cupola. Further ventrally in each nasal passage, a premaxillary artery passes into the nasal vestibule by exiting a canal in the premaxilla, and travels caudally through the layer lining the rostral nasal vestibule and then passes through the cupola to enter the narial erectile mass. Both of these arteries pass through a prominent foramen in the median rostral narial aspect of the premaxilla. Ventral to these foramina is another pair of foramina, each in the ventrolateral narial aspect of the premaxilla. Vessels that exit into the nasal vestibule from these foramina travel caudally into the solum nasi and ramify into the plexus of the ventral vestibule.

Additionally, as alluded to above, the tissue surrounding the walls of the naris and narial canal is highly vascular. In the tissue comprising the medial wall of the narial canal are the large branches of the narial vein, and the narial erectile mass partially forms the rostral and part of the lateral walls of the canal. The narial musculature that contributes to the caudal border of the narial canal and the naris is again highly vascular and seems to contain cavernous vessels.

It is important to note here that we were able to observe through gross dissection a multitude of anastomoses between small arteries and vein in the erectile mass. As in mammalian and avian tissue in the nasal vestibule, the crocodilian “cavernous” tissue does have arteriovenous anastomoses and is thus true erectile tissue.

Dorsal Alveolar Artery The dorsal alveolar canal opens through a large foramen into the caviconchal recess.

The rostral component of the dorsal pterygoideus muscle approaches the caviconchal aperture, and the rostralmost fibers of the muscle reach and attach to the caudal aspect of 320 the recess (Witmer 1995b). The dorsal alveolar neurovascular bundle passes lateral to the

antorbital ( = caviconchal) sinus and continues medial to the lateral aspect of the dorsal

alveolar canal. In this area of its course, the dorsal alveolar artery sends vessels to the

antorbital sinus that ramify and anastomose to form a highly vascular plexus across the sinus.

Just lateral to the caviconchal recess, the neurovascular bundle gives off a dense array of

rostrolaterally oriented, nerve and arterial branches that pass through nutrient canals and exit

to supply the skin. After passing through the caviconchal recess, the neurovascular bundle

travels rostrally across the dorsal aspect of a bony bridge that connects the caviconchal and

postvestibular recesses. The neurovascular bundle then passes through an osseous tunnel

with a strong rostrolateral orientation situated lateral to the postvestibular recess, rather than

traveling through the recess itself. In its course, the bundle grooves the portion of the

maxilla that forms the lateral aspect of the postvestibular canal. A series of three or four fairly large size foramina lines the medial aspect of the canal, and neurovascular branches of the dorsal alveolar neurovasculature pass medially through these and into the postvestibular recess, after which they travel medially to supply the postvestibular sinus. The vessels ramify and anastomose across this sinus to form a dense vascular plexus. On the floor of the postvestibular canal is a foramen situated on the suture between the maxilla and the premaxilla, the ventral subnarial foramen. The ventral subnarial artery and vein, derived from the palatal artery and vein, pass through this foramen and anastomose with the dorsal alveolar vessels.

Upon leaving the postvestibular tunnel, the neurovascular bundle enters into the

paravestibular blood space through a large foramen in the caudolateral blood space. Once

inside the paravestibular blood space, the neurovascular bundle bifurcates into lateral and 321 medial bundles. The lateral paravestibular bundle is located just caudal to the tooth pulp for the large fourth tooth, and contains a large artery and nerve, large veins, and smaller neurovascular structures that exit through nutrient canals to supply the skin. There is a connection between the postvestibular sinus and the mucosa of the solum nasi through an ostium.

The medial paravestibular bundle trifurcates into a rostral premaxillary bundle, a medial bundle, and a caudal bundle, all of which are ensheathed by a thin black tissue which is dorsally covered by an array of mid-sized vessels that travel across it.

The premaxillary neurovascular bundle curves along the medial aspect of the pulp of the fourth tooth, slightly medial to the ridge of bone that define the lateral border of the nasal cavity, and passes into and through an osseous canal in the premaxilla that is continuous with the more caudal area in the maxilla. The premaxillary bundle then bifurcates into rostral and lateral bundles. The lateral premaxillary bundle passes lateral to the fourth tooth root to pass through nutrient canals to supply and innervate the skin of the premaxilla. The rostral premaxillary bundle continues to run against the medial aspect of the lateral ridge of the premaxillary canal, and anastomoses with branches from the lateral premaxillary bundle which forms larger vessels that occupy most of the space within the canal. The rostral premaxillary bundle continues to travel rostrally with a slight rostromedial inclination as it courses along the rostromedial curve of the premaxillary bone. The bundle then splits into a dense array of arteries, nerves, and veins that passes through nutrient canals that supply and innervate the rostral aspects of the premaxilla. After these ramifications, the tunnel becomes ventrally inclined and is filled with large arteries and veins, including large dorsomedially oriented branches that split around the first tooth root, and subsequently pass 322 through large foramina in the now caudal aspect of the premaxillary neurovascular canal which lead into canals that open through the caudomedial premaxilla into the nasal cavity.

These vessels were discussed above in reference to the narial erectile tissue supply.

In the surface of the caudomedial border of the paravestibular blood space is a large foramen, the medial subnarial foramen, that opens medially into the nasal cavity in the caudolateralmost aspect of the nasal vestibule, dorsal to the dorsal surface of the palatal process of the maxilla. The foramen is located in the caudoventromedial aspect of the maxillary process of the premaxilla, just dorsal to the bone’s sutural contact with the rostrodorsomedialmost aspect of the premaxillary process of the maxilla. The medial bundle off the medial paravestibular bundle passes medially through the foramen in the nasal vestibule, and the vessels anastomose with branches from the lateral nasal vasculature

(Rathke 1866; Hochstetter 1906; Reese 1914), as discussed above.

Because of the large anastomosis between the dorsal alveolar artery and the lateral nasal artery via the connecting vessel passing through the medial subnarial canal, several early workers regarded the lateral nasal artery as a terminal branch of the dorsal alveolar artery (Rathke 1866; Hochstetter 1906; Reese 1914). These authors described the dorsal alveolar as curving caudomedially to travel caudally across the roof of the nasal cartilages.

Facial Vascular Plexus and the Narial Erectile Tissue A relatively large, rostrally-facing foramen rests near the rostrodorsomedial aspect of the maxilla, just caudal to the maxilla-premaxilla suture. Though the dorsal surface of the maxilla is covered by small nutrient foramina, the larger rostrally-facing foramen transmits a large branch of the dorsal alveolar artery that travels rostromedially across the surface of the maxilla toward the caudomedial border of the bony naris. Upon reaching the border of the 323 naris, the vessel enters into and significantly contributes to the arterial component of the cavernous vasculature within the caudomedial fleshy naris. The artery that issues from this foramen travels from a canal that opens internally through a foramen located in the rostralmost aspect of the roof of the vascular canal that parallels the postvestibular recess.

Additionally, most of the vast number of nutrient foramina surrounding the bony narial opening send off vessels that course toward and contribute to the fleshy naris. The vessels that course across the dermis of the rough surface of the facial skeleton extensively anastomose and form a plexus that extends across the rostrum, and caudally join a plexus of vessels derived from the nutrient foramina covering the dorsal aspect of the braincase. As a result, the skin of the dorsal portion of the crocodilian head presents a single massive arterial and venous vascular plexus. A large amount of the blood flowing through this plexus has the potential to flow to or from the narial erectile tissue masses via the cavernous vasculature of the external nares. Further caudally, this dermal plexus shares blood with the orbital vasculature and its associated plexuses through anastomotic connections with the supraorbital vessels.

Discussion

The Apomorphic Crocodilian Head In any attempt to reconstruct cephalic vasculature in extinct archosaurs and to trace the evolutionary history of the archosaurian head, Crocodylia is perhaps the least desirable clade to have survived and perhaps the worst possible model. Outside of phytosaurs (which converged upon crocodilians in some ways), non-eusuchian archosaur heads remained fairly conservative over time. Aeotosaurian, sphenosuchian, rauisuchian, and even basal dinosaur

(e.g., Eoraptor and Thecodontosaurus) skulls are similar to each other, and to Euparkeria. The 324 crocodilian head is, deceptively, radically different from the basal archosaurian condition.

Contributing to the highly apomorphic crocodilian head is the fusion of the quadrate and

pterygoid to the braincase, nasal rotation (Witmer 1995b), evolution of a secondary palate

(Ferguson 1981, 1984), and basicranial metamorphosis (Tarsitano 1985). All of these alterations of the ancestral archosaurian head were predicted to greatly influence the structure and pattern of crocodilian head vasculature.

Basicranial metamorphosis involves the verticalization of the basisphenoid and

basioccipital during growth in juvenile crocodilians, both of which have dramatic

consequences for adult head anatomy. In hatchling crocodilians, the floor of the braincase is

flat (Tarsitano 1985). However, during growth, the basisphenoid becomes vertical, and the

braincase floor becomes vertical as a result. Changes resulting from verticalization of the braincase further include the movement of the median pharyngeal ostium to a position dorsal to the secondary choanae, and the closure of the connection between the basioccipital

and basisphenoid sinuses. During basicranial metamorphosis, the pterygoid is pulled to a

position closer to the occiput, which changes the orientation of the jaw muscles.

Additionally, the ventral aspect of the quadrate is pulled dorsally to a position where it

extends caudally beyond the occiput. Possibly related to basicranial metamorphosis is the

fusion of the quadrate and pterygoid to the braincase. In crocodilians the quadrate nearly

completely covers the lateral surface of the prootic (Iordansky 1973).

Witmer (1995b) recognized the process of nasal rotation as another important

developmental feature with major implications for crocodilian head anatomy. Nasal rotation

is a process where the nasal capsule, and the tissues associated with it, internally rotate

during development. The process occurs over ontogeny and tends to follow a rostral (e.g., 325 the nares) to caudal (e.g., the lacrimal) sequence. With nasal rotation, structures that were lateral in ancestral archosaurs become dorsal in eusuchians. Witmer (1995b, 1997) reported evidence for the first appearance of nasal rotation in Neosuchia.

In view of the profound morphological evolution of the head in Crocodylia and the developmental processes that result in the phenotype, the most striking finding of this research is the extreme similarity between vascular structures and patterns in birds and crocodilians. Throughout every anatomical region of the crocodilian head, clear similarities can be found between the blood vessels of birds and crocodilians, including the vessel’s parent vessel, the branches of the vessel, the objects of supply of the vessel, and the bony and soft-tissue relationships of the vessel (including the objects the vessel passes through or near).

In Chapter 2, I discussed clear osteological correlates for encephalic vessels in birds and crocodiles, and archosaurs in general. I further discussed the osteological correlates for the physiologically significant nasal vestibular vascular plexus in amniotes.

The nasal vestibular vascular plexus (NVVP) and many of the encephalic vessels demonstrated close relationships between particular bones and blood vessels. However, as with bone-blood vessel-brain-dura interrelationships, birds and crocodiles consistently demonstrated similar, complicated relationships between diverse anatomical elements within and/or across regions. For example, in all birds and crocodilians studied, the external carotid artery bifurcates into the temporomandibular and oromandibular arteries along the caudodorsal surface of m. pterygoideus ventralis near the muscle’s insertion into the internal mandibular process, and the first branches of the oromandibular trunk supply m. depressor mandibulae. There are numerous other “functional matrices (Moss 1971)” in crocodilians 326 and birds involving close interconnected relationships between bone, muscle, nerves, and blood vessels, and it could be argued that the osteological correlates for non-vascular tissue are then indirect correlates for blood vessels or vascular patterns. In the above example, the internal mandibular process, an unlikely vascular correlate, would actually imply the course of the oromandibular and temporomandibular arteries, the area of their origin from a common trunk, and the structures they immediately supply (mm. pterygoideus ventralis and depressor mandibulae).

Rather than discuss commonality of vascular structure and pattern, given the degree of similarity and potential homologies between both extant archosaur clades, this section will discuss areas where crocodilians differ from birds.

Stapedial System Perhaps the most obvious difference between the cephalic vasculature of Crocodylia and Aves is the origin of the stapedial artery. In crocodilians, the stapedial artery is a proximal branch of the external carotid artery, whereas in birds, the stapedial artery is a proximal branch of the internal carotid artery. However, the course and branching pattern of the stapedial artery in birds and crocodilians are very similar. Interestingly, in both groups, the first substantial branch of the vessel is the acoustic artery, and in both groups the latter vessel forms an erectile tissue system or organ in the middle ear cavity. The stapedial arterial system has several clear osteological correlates (see Table 4) that are shared in both extant archosaur clades, and these correlates relate to several regions (e.g., parabasal fossa, temporal region, orbit) along the pathway of the vessel and its branches. The fortuitously large number of osteological correlates for the stapedial system allows for fairly detailed reconstruction in fossil specimens. 327 Beyond the origin of the stapedial artery, I identified four major vessels in

crocodilians with an anatomy that differed substantially from avian anatomy.

(1) External Occipital Artery Archosaurs possess a foramen between the squamosal dorsolaterally and medially,

the paroccipital process ventrolaterally, the supraoccipital ventromedially, and the parietal

dorsomedially. In birds this foramen transmits the external occipital artery. The external

occipital artery branches from the temporoorbital artery just rostral to the latter vessel’s exit

from the cranioquadrate canal. The external occipital artery then travels through a canal in

the floor of the dorsal tympanic recess. In its proximal path, the vessel partly travels across

the dorsal aspect of the prootic, and distally across the dorsal surface of the supraoccipital.

Oddly, a similar canal does exit in extant crocodilians. Caudal to its entrance into the

cranioquadrate canal, within the middle ear space, the crocodilian temporoorbital artery

travels across the dorsal surface of the prootic. The caudal aspect of this part of the prootic

slopes caudomedially and is sutured to the dorsomedial aspect of the supraoccipital, and the

latter bone has a smooth surface that ends as the floor of an “external carotid artery” canal.

Thus, a typically avian canal for the external carotid artery exists in crocodilians. However,

no temporoorbital artery in any alligatorid or crocodylid dissected in this study sends off an

external occipital artery, and no vessel passes through this canal. Moreover, the “external

occipital foramen” is walled over by connective tissue that occasionally and partially ossifies

in adults.

(2) External Occipital Vein In extant crocodilians, a diverticulum of the tympanic cavity infiltrates the basioccipital, expands into the otoccipital, and then enters into the supraoccipital. The supraoccipital is 328 then highly pneumatic, and “inflated” by this sinus. A pneumatic foramen is situated in the

lateral aspects of the supraoccipital, and these foramina open into the right and left middle

ear spaces, respectively. In juvenile and adult crocodilians the sinus in the supraoccipital

expands across the midline to form an “intertympanic” sinus.

In birds and all non-crocodiliform fossil archosaurs analyzed in this study, the rostral

petrosal sinus and its caudodorsal extension, the rostral semicircular vein, send off a

prominent branch, the external occipital vein, which exits the endocranial cavity through a

foramen in the rostrodorsomedial surface of the supraoccipital. The vein then travels,

almost directly, through a short canal and exits into the external occipital region through a

foramen located between the supraoccipital and the exoccipital. In crocodylids (and

apparently Gavialis) there is a cluster of small foramina in the rostrodorsomedial surface of the supraoccipital, along the distal component of the sulcus for the rostral petrosal-rostral semicircular vein. The veins that pass through these foramina enter into the air space within the supraoccipital and drain into the extensive network of venous vasculature across the

“intertympanic” sinus. Because of the large air space in the supraoccipital, the external

occipital vein never exits the bone. In alligatorids, no detectable foramina in the rostrodorsal

supraoccipital or within the rostral petrosal sinus sulcus link the inner supraoccipital with the

endocranium. The external occipital vein has thus been greatly reduced in extant crocodylids

and apparently lost in extant alligatorids.

(3) Cerebral Ophthalmic Artery In birds, the cerebral ophthalmic artery is the ventral branch off the rostral cerebral

artery) and travels through the endocranial region dorsal to the optic foramen and then exits

through a foramen in the orbitosphenoid (Richards, 1967; Baumel 1975, 1993; Chapter 2). 329 In the orbital aspect, the foramen is dorsal to the rostral aspect of the optic foramen. The foramen is typically far rostrodorsal from the trochlear nerve foramen and is not likely to be mistaken for it. Often, a deep groove for the cerebral ophthalmic artery extends rostrodorsally across the orbitosphenoid to the olfactory sulcus, which presents an osteological correlate for the cerebral ethmoid-ethmoid + supraorbital artery anastomosis.

No such foramen could be identified in the laterosphenoid or interorbital septum of extant crocodilians. Moreover, in all studied crocodilians, the rostral cerebral artery does not send off a ventral, or any other, vessel that travels into the orbit. These findings are in agreement with Hochstetter (1906) and Shiino (1914), although Rathke (1866) did identify such a vessel in crocodilians.

The avian cerebral ophthalmic artery anastomoses with the ophthalmotemporal artery, and the resulting vessel anastomoses with the supraorbital and ethmoid arteries.

Thus, the cerebral ophthalmic artery is an important component of both a system of orbit- brain interconnections and connections between the cerebral carotid and stapedial arterial systems. The cerebral ophthalmic artery potentially provides a direct route for blood in the orbit to reach the cerebrum, and from the cerebral vasculature to reach the rest of the brain.

Similarly, the temperature of the blood to the cerebrum could be effected by the cerebral ophthalmic artery which has connections to various orbital and extra-orbital vascular physiological devices (e.g., ciliary and choroid plexuses and the ophthalmic rete).

Additionally, the blood in the artery can reach the brain through a series of less direct routes

(e.g., through its indirect anastomosis with the ethmoid artery). In light of these connections and their association with orbital vascular physiological devices, the cerebral ophthalmic artery has significance beyond the movement of nutrients into the orbit, including a potential 330 role in brain cooling. For example, distal to sending off a series of branches to the

Harderian gland, the terminal element of the ophthalmotemporal artery joins the cerebral ophthalmic artery. As discussed below, the Harderian gland is a potential endocrine organ, and does secrete various compounds and products into the circulation (e.g., melatonin). In birds, the cerebral ophthalmic artery is a potential conduit for Harderian gland products to the cerebrum, and, less directly, the epiphysis gland, hypothalamus, and other brain areas via the encephalic arterial system.

Because the osteological correlate for the cerebral ethmoid artery is located in the orbitosphenoid or rostrodorsal laterosphenoid and the orbitosphenoid is only variably ossified in birds and infrequently ossified in non-avian archosaurs, the cerebral ophthalmic artery is difficult to reconstruct in fossil forms. However, there are fossil archosaurs that do seem to have a cerebral ethmoid artery foramen. Such a foramen is found in Sphenosuchus acutus, in the far rostrodorsal surface of the laterosphenoid, just rostral to the dorsal aspect of the cotylar crest, and far rostrodorsal to the trochlear foramen. A cerebral ethmoid artery was identified in the (extremely) basal archosaur Proterosuchus by Clarke et al. (1993) in a position quite similar to the avian foramen, and I was able to confirm this observation in two

Proterosuchus specimens.

It is important to note that archosaur orbits are frequently characterized by an

“orbitocranial” fenestra in the caudodorsal aspect of the orbit. The fenestra is within the rostral laterosphenoid or caudal orbitosphenoid, and is lined by a membrane. In extant crocodilians, the fenestra can occur rostral to the rostrodorsal aspect of the laterosphenoid.

In birds it is located in the caudodorsal orbitosphenoid (it is of course difficult, if not impossible, to differentiate between orbitosphenoid and laterosphenoid in this area). In 331 Proterosuchus and Sphenosuchus, there is another foramen located caudal to the cerebral

ophthalmic and dorsal to the trochlear foramina, and is particularly large in Sphenosuchus.

However, in Sphenosuchus the foramen is caudal to the cotylar crest, whereas it is rostral to the

crest in Proterosuchus. Clarke et al. (1993) interpret these foramina as for the “ophthalmic

artery,” but they are in the position of an orbitocranial fenestra, and a foramen for the

cerebral ophthalmic already exists. In Euparkeria a very large fenestra is located rostral to the

cotylar ridge and rostrodorsal to the optic nerve foramen in the rostrodorsal laterosphenoid.

A small foramen rests caudodorsal to the fenestra and rostrodorsal to the optic nerve notch,

and is a good candidate for a cerebral ophthalmic artery foramen. A trochlear foramen is

situated far caudoventrally in a position caudodorsal to the optic nerve notch.

Based upon birds and Sphenosuchus, the cerebral ophthalmic artery would have been

present in the ancestral avesuchian, and was present in the avesuchian outgroup

Euparkeriidae. Based upon Proterosuchus, the trait would have been present in the ancestral

archosaur. Archosauromorph outgroups to Archosauria, including rhynchosaurs and

protorosaurs, do not ossify the laterosphenoid or orbitosphenoid, preventing the

identification of the foramen. I could not identify an external ophthalmic artery foramen in

Desmatosuchus, a member of the crocodylomorph outgroup Aetosauria. However, it is

probable that the area of the orbitosphenoid with the foramen was not ossified in the

representatives of this species that I studied. It is important to note that Sphenosuchus is a basal crocodylomorph; thus, the artery persisted into at least the basal branches of this clade.

Crocodilians apparently compensate for the lack of a cerebral ethmoid artery through

the rostral branch of the trigeminal artery. As discussed in the results section, the latter

artery travels through the profundal canal and ramifies into a series of vessels in the orbit. A 332 prominent branch of the artery joins the ventral branch of the ophthalmotemporal artery

before the latter vessel anastomoses with the orbital artery. After joining the orbital artery,

the ventral branch of the ophthalmotemporal artery continues to supply the Harderian

gland. The lateral ramus of the trigeminal artery originates from the joining of vessels from

the caudal encephalic and basilar arteries. Thus, the crocodilian lateral branch of the

trigeminal artery acts as a connecting vessel between the orbit and the encephalic cavity, and,

similar to birds, joins with the ophthalmotemporal artery near the latter vessel’s supply to the

Harderian gland. Interestingly, this artery apparently does not exist in birds.

(4) Sphenoid Artery In birds the internal carotid artery sends off two medium sized vessels, the

sphenopalatine and sphenomaxillary arteries that eventually travel ventral and dorsal to the

basipterygoid process, respectively. As described in the results section, the crocodilian

sphenoid artery (arteries) is quite reduced, and only becomes large upon anastomosis with

the lateral ramus of the trigeminal artery. In at least one specimen, two small caliber vessels

traveled through the CN VIIp canal, and there are apparently two vessels that anastomose

with the trigeminal vessels. Upon anastomosing with these vessels, the larger sphenoid

artery divides into a branch that courses to the nasal cavity and a branch that travels to the palate with its respective nerves, and additionally, the anastomotic vessels course into the orbit and anastomose with the orbital vasculature.

In basal archosaurs (e.g., Proterosuchus, Erythrosuchus, Euparkeria), the cerebral carotid foramen is located within a sulcus for the palatine ramus of the facial nerve in the lateral aspect of the ventral surface of the basisphenoid, dorsomedial and slightly caudal to the basipterygoid process. The groove originates just rostroventral to the facial nerve foramen. 333

Rostral to the cerebral carotid artery foramen, the CN VIIp groove then courses rostrodorsally around the basipterygoid process to the caudoventrolateral aspect of the parabasisphenoid rostrum, and then continues along the ventrolateral surface of the rostrum.

In avesuchians, including basal ornithodirans and suchians, the cerebral carotid artery

foramen is situated in the dorsolateral aspect of the basisphenoid within the CN VIIp sulcus in a position caudodorsomedial to the basipterygoid process. Distal to the foramen, the sulcus travels rostroventrally toward the basipterygoid process and then divides around the process. A dorsal groove curves rostrodorsally around the process to the dorsomedial surface of the process. A ventral groove curves rostroventromedially around the process to the rostromedial aspect of the process and the caudoventrolateral surface of the parabasisphenoid rostrum. Thus, in avesuchians, a clear osteological correlate exists for the

course of CN VIIp and its bifurcation into its dorsal and ventral divisions. As the cerebral carotid artery foramen rests within the sulcus, it seems likely that a branch(es) of the vessel traveled with the nerve and divides with it into the sphenomaxillary and sphenopalatine arteries, or alternatively the cerebral carotid artery sends off two separate vessels, the sphenomaxillary and sphenopalatine arteries that then travel through the sulcus and divided around the basipterygoid process. The grooves for the various neurovascular bundles are quite large and deep, which may indicate large vessels on par with the avian condition.

A “pterygoid” or “sphenoid” canal has convergently evolved in birds and crocodilians. In crocodilians, as previously discussed, the caudal aspect of the canal is formed by (1) the union of a rostroventral process of the basipterygoid process with a caudoventral process of the rostrum that forms the lateral wall of the canal, (2) the basisphenoid that forms the medial wall of the canal, (3) and the basipterygoid process that 334 forms the floor. This caudal component of the canal is really a foramen that opens into the

rostral component. The rostral component is formed by the lateral aspect of the rostrum

medially, the dorsomedial surface of the pterygoid ventrally, and the expanded quadrate

process of the pterygoid process laterally. The canal opens through a slit between the

rostromedial quadrate process and the caudoventrolateral rostrum. In birds, the sphenoid

vessels pass through a tunnel within the basiparasphenoid that ends in foramina caudodorsal

to the basipterygoid process.

Palatine Vasculature, Gaping Behavior, and Gular Flutter Gaping is a behavior exhibited by crocodilians where the mouth is held open to

expose the moist oral mucosa to air. Though earlier studies had failed to find a

thermoregulatory function for this behavior (e.g., Diefenbach 1975), Spotila et al. (1977)

demonstrated that gaping significantly slowed the rate of heat gain in the head region and

that thermal time constants were much higher in gaping alligators than in those with closed

mouths. A later study (Brown and Loveridge 1981) was able to show that gaping does cause

evaporation of water from the oral mucosa. However, it is not known how heat is

transferred from the brain region to the mouth. In their paper, Spotila et al. (1977) stated

“heat may be transferred by direct conduction of the bony skull/or by blood circulation definitive comments on mechanisms within the alligator cannot be made until further investigations of vascular patterns, conduction pathways, and the mechanics of heat flow within the head have been carried out.” A step in this direction was provided by Ferguson

(1984) who described a palatal vascular plexus formed by two arteries entering the caudolateral palatal mucosa and branching into multiple transverse and longitudinal vessels that anastomose with one another and a single mid-line vessel. 335 This study has attempted to elaborate on the current knowledge of the palatal plexus.

The plexus is fed by lateral arteries entering the caudolateral palatal submucosa from the

palatine artery, a ventral branch of the palatomaxillary artery. Additionally, dorsal branches of these vessels pass through a longitudinal series of foramina in the maxilla just medial to the tooth row which anastomose with ventral branches of the dorsal alveolar artery. An important osteological correlate is a ventrally placed foramen, the ventral subnarial foramen,

at the premaxillary-maxillary suture which transports a vessel from the palatine artery that

anastomoses with branches of the dorsal alveolar artery within the postvestibular recess; the

products of this anastomosis then pass into the paravestibular blood space of the premaxilla

and exit the medial (or vestibular) “subnarial” foramen. Thus, the buccopharyngeal plexus

(discussed below) has a direct connection with the nasal vestibular vascular plexus (see

Chapter 2).

Perhaps a more intriguing aspect of gaping is its reported association with gular flutter in crocodilians. Gular flutter is a widespread avian behavior by which the mouth is held open

(gaping) and fluttering occurs in the gular area (e.g., esophageal pulsation) to enhance evaporation of water from the submucosal oropharynx and esophagus. Anatomical correlates common to many birds for gular flutter include plexiform veins in the soft palate and post-glottal larynx, huge interjugular anastomosis in the roof of the esophageal inlet, and possibly arteriovenous anastomoses (AVA’s) in the oropharynx (Baumel et al. 1983)

Gular flutter has been identified in members of Pelicanifiormes, Cuculiformes,

Ardeidae, Columbiformes, Caprimulgiformes, and Strigiformes (Lasiewski and Bartholomew

1966). As ambient temperature increases, the cost of panting in birds becomes too high

because of excessive water loss, and the bird ultimately suffers from heat stroke (Lasiewski 336 and Bartholomew 1966). However, gular flutter has low energetic costs, and birds that use gular flutter are capable of maintaining low body temperature in response to increasing ambient temperature (Lasiewski and Bartholomew 1966). A study of the poor-will, a caprimulgiform that uses gular flutter, found that the bird begin to flutter around 30ºC, that flutter increased with temperature, and that flutter was mechanically based upon the resonating frequency of the hyobranchial apparatus (Lasiewski and Bartholomew 1966).

Moreover, the authors determined that during gular flutter heart rate increased and that the arteries in the buccal region swelled with blood. Throughout the experiment, the birds maintained a gular temperature 3ºC lower than core body temperature.

This study has discovered a plexus of anastomosing arteries within the submucosa of the pharynx just caudal to the choanae supplied by pharyngeal branches of the submandibuar artery (that dorsally anastomoses into the palatal plexus), that pass over the ventral aspect of the ectopterygoid before reaching the choanae and vessels derived from the lingual branch of the external carotid artery. More interesting are a pair of large lateral diverticula of the pharynx caudal to the choanae and caudolateral to the median pharyngeal pouch that are fed by a very dense plexus of anastomosing arteries. Moreover, these diverticula are situated immediately ventral to the internal carotid arteries whose first branches are the cerebral carotids which directly supply the brain. The vasculature of this region is even more extensive, and will be discussed as a system toward the end of the discussion.

Elements of the Circumpharyngeal Ring The archosaurian buccopharyngeal plexus, as identified in birds and crocodilians, consists of a circumpharyngeal ring of dense vasculature linked by large vascular 337 plexuses. There are six large vascular physiological devices in the circumpharyngeal

ring. Dorsally, the buccopharyngeal network consists of the following.

(1) The palate. In both birds and crocodilians a plexus of tightly compacted anastomosing arteries and veins is concentrated along the submucosa of the ventrolateral maxilla. Midtgard (1984a) recognized that the lateral aspect of the palate had the highest density of vessels in mallards, and this is similarly the case in crocodilians. It is important to note that large palatine glands rest across the ventrolateral surface of the maxilla in birds (McLelland 1993) and crocodilians (Reese

1924), and that a large component of the lateral palatine vascular plexus likely supplies and drains these glands. In bird and crocodilians, the lateral palatine plexus is largely supplied by the palatine artery, which is a branch of the proper maxillary artery in crocodilians and ratites and is a branch of the pterygoid + submandibular + sphenomaxillary arterial anastomosis in galloanserines.

Branches from the lateral plexus stretch medially across the palate to form a

looser, centrally located arterial plexus. Again, in birds and crocodilians, a single median artery is located across the longitudinal axis of the palate and sends off medial vessels that ramify into the lateral plexus. The median palatine artery results from the right and left anastomosis of terminal branches of the proper maxillary artery system in ratites, and the anastomosis of terminal branches of the submandibular arterial system in galloanserines. The origin of the vessel in crocodilians is unclear.

(2) The secondary choanae. The choana is surrounded by a thickening of

mucosa, the choanal torus, that is extremely vascular in crocodilians and birds and is 338 connected to the pterygoid plexus. In both groups, the choana receives a diverse blood supply, mainly from the sphenopalatine artery in birds, but also receiving blood from branches of the oromandibular artery. This plexus extends caudally to supply and drain the area of the tissues of the median pharyngeal and lateral pharygotympanic tubes and interconnects with the plexus of the lateral pharygeal diverticulum.

(3) The pterygoid plexus. A fine and occasionally dense network of vessels extends across the submucosa of the ventral pterygoid. Corrosion casts of crocodilians demonstrate a wide plexus of relatively large, anastomosing veins. The sphenopalatine and submandibular arteries typically supply this region. Dorsally, branches from the plexus anastomose with branches from the pterygoid artery that course along the dorsolateral surface of the pterygoid and can anastomose with branches from the palatine and proper maxillary arteries. Arteries from this network contribute to the arterial plexus surrounding the maxillary vein.

(4) Lateral pharyngeal diverticulum. As discussed in the results section, in crocodilians, the dorsolateral pharynx produces a thick mucosal diverticulum associated with a cavernous-tissue like vascular network with arteriovenous anastomoses. Perhaps significantly, this pharyngeal diverticulum rests against and is partially supplied by the internal carotid artery, just proximal to the entrance of the artery’s entrance into the external ostium of the cranial carotid canal. Thus, the anatomy of this structure is analogous to the equid guttural pouch (Baptiste 1998), which is further discussed in Chapter 2.

Ventrally, the buccopharyngeal network consists of the following. 339 (1) The tongue. The tongue consists of a venous and an arterial vascular plexus.

In ducks, the venous plexus is concentrated along its lateral aspects (Midtgard

1984a), and this is similarly the case in galliforms. In corrosion casts of crocodilians,

the tongue appears as a flat and expansive venous and arterial network. In both

archosaur groups, the arterial plexus is mainly supplied by the proper lingual artery.

(2) The mons laryngis. In both archsosaur groups, the submucosa and musculature of the mons laryngis is extremely vascular, and forms an arterial and venous plexus. The cavum laryngis contains a complex array of mucosa lined fossae that contain extensions of the mons laryngis plexus. The plexus is supplied by the laryngeal artery, anastomoses with the vascular supply to the trachea, and is laterally connected in crocodilians to the highly vascular cavum pharyngis.

Obviously, the ventral component of the buccopharyngeal network is intimately

associated with the hyobranchial apparatus, and will be directly mechanically manipulated

during gular flutter.

Cephalic Vasculature and the Epiphysis-Harderian Gland-Hypothalamus Axis Crocodilians are, beside xenarthrans and manatees, thought to be the only

vertebrates that do not have a epiphysis gland (Quay 1979; Butler and Hodos 1996). An

important question then is: how are circadian rhythms regulated in crocodilians?

Crocodilians do exhibit circadian rhythms. Additionally, the rhythm reported in

alligators appears to be regulated by light rather than temperature (Lang 1976), although other research has determined the rhythm to be regulated by extraretinal light but dependent upon temperature (Kavaliers 1980; Kavaliers et al. 1981). Throughout the year, juvenile alligators leave water at sunrise and then move back into the water at sunset (Lang 1976). 340 These behaviors could be manipulated by artificial light (Lang 1976; Kavaliers et al. 1981), but the change occurred gradually indicating an endogenous rhythm. It is also important to note that the behaviors were not thermoregulatory and that in the mornings the alligators moved from a warmer area (the water) to a cooler one, and again at sunset the alligators moved from a warmer terrestrial environment to cooler water, and both behaviors resulted in a 3.0ºC body temperature decrease.

In crocodilians and birds the ophthalmotemporal artery and vein anastomose with the ethmoid artery and vein distal to supplying or draining the Harderian gland. The ethmoid arteries are branches of the rostral cerebral vessels that interconnect to the rest of the brain’s blood supply. The anastomosis between the rostral cerebral arteries may additionally provide a partially closed circuit for the movement of blood through the cerebrum. In birds, the ophthalmotemporal artery has an additional connection to the rostral cerebral artery via the cerebral ophthalmic artery, and in crocodilians, the lateral trigeminal artery connects the ophthalmotemporal artery to the caudal encephalic vasculature, and thus, the rhombencephalon. Of possibly greater significance, the orbital artery and vein connect the vasculature of the Harderian gland to the hypophysis blood supply and the cavernous sinus surrounding the hypophysis, respectively.

In an important study that first demonstrated the complex and important role(s) played by the Harderian gland, Wetterberg et al. (1970a) found that removal of the

Harderian gland in rats eliminated the effect of light on the circadian levels of serotonin.

The authors identified porphyrins, photosensitive pigments, in the gland, which make it an extra-retinal photoreceptor. In a subsequent paper, Wetterberg et al. (1970b) determined that removal of the Harderian gland eliminated the rhythmic levels of epiphysis 341 hydroxyindol-O-methyltransferase (HIOMT), an enzyme related to the production of

melatonin, and which typically increases at midnight and has a nadir at the end of the light

period. Thus, the Harderian gland was found to seemingly exert control over the epiphysis

gland.

Biological Importance of Melatonin Melatonin is secreted by the Harderain gland in several amniote species (see below).

The following discussion concerns the biological importance of melatonin. If melatonin is

secreted from the Harderian gland in both birds and crocodilians, then the gland and its

blood supply can be viewed as important influences on archosaur biology.

In the Indian jungle bush quail Perdicula asaiatica, an inverse relationship associated with the reproductive cycle was found between adrenalin, corticosterone, plasma testoserone

/estradiol and epiphysis gland weight and plasma melatonin levels (Sudhakumaria et al.

2001). Adrenal weights were highest in June during the reproductive phase, and cortical cell height increased during this period. Adrenal and gonad weights were lowest in December, the reproductive inactive phase, and adrenal cells atrophied as possessed fewer mitochondria. The adrenal gland paralleled gonad weight to the recrudescence phase

(March-May). Epiphysis weight was highest from November to December, and lowest from

May to June. Thus, the epiphysis gland inhibited adrenal and gonad growth, and a decrease in epiphysis activity was followed by the seasonal growth of the gonads and adrenal gland

(Sudhakumaria et al. 2001).

A thermocycle was identified in a gecko (Christinus marmoratus) where an increase in melatonin occurred during cooler periods and during a dark phase (Moyer et al. 1997).

Melatonin decreased during the light phase. The authors found that a spike in temperature 342 was required for cycle onset, and that temperature may be the Zeitgeber for nocturnal ectotherms.

In a comparative study of the relationship between melatonin and body temperature in house sparrows, owls, and Japanese quail, body temperature was found to decrease in all birds after an injection of melatonin (Murakami et al. 2001). In both the diurnal sparrow and the quail, the melatonin injection prevented body movement, but did not prevent movement in the nocturnal owl. Thus, the diurnal circadian rhythm was found to control both body temperature and movement in the two diurnal birds, whereas only body temperature was controlled in the owl. However, the epiphysis gland is considered “degenerate” in most owls, and strigiformes typically have low plasma melatonin levels (Murakami et al. 2001).

The first well developed epiphysis gland found in an owl was in the tropical and nocturnal species Athene brama (Haldar and Guchhait 2000). The epiphysis gland was found to be both triangular and large as in diurnal birds, and like diurnal birds, the gland was characterized by perivascular sympathetic nerves that innervated it. Unlike temperate owls, melatonin was highest during the reproductive phase and lowest during the reproductive inactive phase.

Male starlings experience a reproductive cycle with a stage of testicular growth, then testicular regression, followed by molt, and then a second stage of testicular growth

(Gwinner and Dittami 1980). The authors found that epiphysisectomy resulted in earlier testicular regression and the loss of the second stage of second growth.

Ching et al. (1999) identified melatonin receptors in the salt gland of Anas platyrhynchos. The authors found that melatonin decreases salt gland secretion. Typically, salt water intake leads to an increase in NaCl in the plasma, stimulating hypothalamic 343 osmoreceptors that signal secretion from the gland via parasympathetic nerves. Since

melatonin actually stimulates the parasympathetic pathway, the authors concluded melatonin

could inhibit secretion via this pathway. A proportional relationship between salt gland

secretion and blood flow was found, and melatonin has been found to cause

vasoconstriction in other organs. Thus, melatonin might reduce salt gland secretion via

vasoconstriction of the blood supply to the gland.

Melatonin was identified in the pigeon duodenum, epiphysis gland, choroid plexus,

hypothalamus, and Harderian gland (Vakkuri et al. 1985). The pigeon melatonin levels

demonstrated a rhythm with diurnal variation, being significantly higher at midnight and

lowest at midday.

Melatonin synthesis has been demonstrated in the retina of trout, making it a true

endocrine organ, and is the first known source of extra-epiphysis melatonin (Gern and Ralph

1979). The melatonin is synthesized from a serotonin substrate. The trout retina releases

the melatonin into the blood vascular system.

Innervation of the Harderian Gland Blood Vessels Axons of postganglionic fibers from the pterygopalatine ganglion to the orbital choroidal vessels in pigeons were found to contain VIP+ (vasoactive intestinal polypeptide), nNOS (nitric oxide), and NADPH-diaphorase+ (Cuthbertson et al. 1997). VIP and nNOS

were all found in the pterygopalatine ganglion.

Cuthbertson et al. (1997) identified three to four pterygopalatine ganglia, and many

lesser ganglia, along the dorsal aspect of the Harderian gland, and even more fibers and

ganglia encircling the dorsal, medial, and lateral aspect of the gland. The two largest ganglia

rested on the dorsal surface of the gland, with the rostral microganglion along the 344 rostrodorsal aspect and the caudal microganglion on the caudodorsal aspect of the gland.

The authors mentioned that interconnected ganglia have also been identified around the

Harderian gland in Anser.

This study identified a larger apparent ganglion along the dorsal aspect of the caudal

tail of the crocodilian Harderian gland, and identified a similarly sized ganglion along the

caudodorsal aspect of the main body of the gland. Similarly, several smaller potential ganglia

were identified near the gland.

The fibers issuing from the various ganglia formed a plexus, and fibers containing

VIP+, NADPH-diaphorase+, and nNOS traveled to and joined the profundus nerve which

courses dorsal to the gland (Cuthbertson et al. 1997). Fibers containing NADPH traveled to

and joined the ventral ramus of CN III. Several fibers traveled to the blood vessels, derived

form the ophthalmotemporal artery, in the vicinity. The latter fibers, carrying VIP+,

NADPH-diaphorase+, and nNOS , traveled along the vessels to the choroid.

Again, this study identified in Alligator numerous fibers traveling from the various

apparent ganglia to branches of the ophthalmotemporal artery and vein. These fibers

traveled caudally along the vessels, and then traveled to branches of the ophthalmotemporal

vessels involved with supplying and draining the choroidal plexus. Additional fibers traveled

along the vessels supplying and draining the Harderian gland.

VIP+ and nNOS are vasodilators, and Cuthbertson et al. (1997) hypothesized that they are used to control blood flow in and out of the choroid plexus and Harderian gland through vasodilation. According to Cuthbertson et al. (1997), mammals also use VIP+ and nNOS to control the choroidal blood vessels, and in mammals NO actually sets the basal flow rate. Unlike birds, the mammalian pterygopalatine ganglion does not consist of a series 345 of interconnected ganglia. The authors hypothesized that control of choroidal vasodilation is used to increase the nutrient supply to the retina and to thermoregulate the retina in birds.

Unmylinated nerve fibers travel in the lobular aspect of the Harderian gland along blood vessels in rats (Bucana and Nadakavukaren 1972) and in the Aylesbury duck

(Fourman and Ballantyne 1967). In the latter, it was proposed that the secretory activity of the gland was dependent on blood flow to the gland.

In mice, rats, and humans, sympathetic fibers traveling from the superior cervical ganglion divide into lateral and medial branches within the endocranium (Maklad et al.

2001). The medial branch joins with the greater petrosal nerve to form the nerve of the pterygoid canal. Sympathetic fibers from the nerve of the pterygoid canal enter into the skull by passing through an un-named foramen in the basisphenoid, and then “join” CN’s III, V,

IV in an area medial to the trigeminal ganglion. Fibers from the medial branch travel directly to the abducens nerve and then travel along CN VI. Fibers traveling with CN VI ultimately travel from the nerve to join CN’s III, IV, the maxillary nerve, and the profundus nerve.

Moreover, fibers associated with the abducens nerve form a huge plexus around the trigeminal ganglion. Most of sympathetic nerves traveling with CN VI join the lacrimal and nasociliary branches of the profundus nerve. Sympathetic fibers had to use CN VI to travel to the profundus nerve. The fibers that remain with CN VI are thought to travel to the blood vessels in m. rectus lateralis. The sympathetic fibers were found by Maklad et al.

(2001) to travel rostrally and caudally along the nerves they joined, and some of the fibers that traveled to the trochlear nerve then traveled caudally along the nerve to the tentorium cerebelli to innervate the epiphysis gland (that is strongly regulated by sympathetic nerves). 346 The authors mention previous studies finding that the parasympathetic fibers also use the abducens nerve as a central means of transit.

Though all of the organisms use in the above study are of but a single clade of mammals, this research does agree with my gross observations in Alligator that fibers from the palatine ramus of the facial nerve apparantly use the abducens nerve as an early, and major, transit system to reach the ciliary plexus and the vasculature of the Harderian gland.

In birds, however, CN VIIp traveled to the Harderian gland by coursing along the eye’s and the gland’s venous drainage (the ophthalmic vein).

Functions of the Harderian Gland A series of studies have identified a close relationship between the Harderian gland and the vomeronasal organ in squamates (Rehorek et al. 1999, 2000a, b, and c; Hillenius et al. 2001). However, extant archosaurs do not have a vomeronasal organ. Additionally, amongst squamates, the Harderian gland has been found to produce lipids only in geckos

(Rehorek 1997).

Djeridane (1994) identified arginine vasopressin (AVP) in the rat retina, and the lacrimal and Harderian glands, and AVP levels experienced circadian fluctuations. The AVP was located in the ganglion cells of the retina and in the excretory ducts of the glands. AVP was also identified in the rat epiphysis gland. AVP is known to contribute to osmotic balance and has been found to increase with exercise (e.g., running) in rats

(Ghaemmanghami 1987). Djeridane (1994) further described a rich blood vascular system in the rat Harderian gland that was comprised of fenestrated capillaries that would allow for the release of AVP. 347 Dubey and Haldar (1997) found a strong relationship between the Harderian gland, seasonal change, and the reproductive cycle in Indian jungle bush quail. In late May, the ovary and Harderian gland increase in mass, whereas the epiphysis gland decreases in size.

Also in late May, the porphyrin content in the Harderian gland increases. Late May characterized by long days, mild humidity, and higher temperatures. In July, humidity begins to increase and Harderian gland mass decreases. A second peak in gland mass was found in

October and again in January, both of which featured a transition in day length and temperature, but had mild humidity. As plasma melatonin decreased, plasma extradiol increased.

A sex hormone influence on the Harderian gland was reported by Gupta and Maiti

(1983) in ducks. In females, extradiol increased mitosis in the Harderian gland, but cell size and the mucous substance decreased. In males, extradiol increased mitosis and cellular breakdown.

In Gallus and Anas, androgen, estrogen, and progestin receptors have been found in the Harderian gland (Vilichis et al. 1991). The former two receptors are known in mammal

Harderian glands, but progestin is not. Chickens have significantly more androgen receptors than do ducks.

There is strong evidence that the avian Harderian gland is an important

immunological organ. Lymphoctytes were identified in the lacrimal and Harderian glands

and ducts (Burns and Maxwell 1979) in Gallus, Meleagris, and Anas. Two populations of

lymphoid cells were found in the Harderian duct. Antibody formation against particulate

and against antigens (Burns 1976) has been reported in the Gallus Harderian gland. Burns

(1977) identified the Harderian gland as a route of antigen uptake. Immunoglobulins IgA, 348 IgG, and IgM have been further described in the Harderian gland of Gallus (Burns 1992), and Burns asserted that this gland possesses more plasma cells than any other organ in the chicken.

Payne (1994) emphasized that the vertebrate Harderian gland can produce four major products: (1) mucous secretions (in birds, Slonaker 1918); (2) lipids (in avian type 1 gland; Burns 1992), that are potentially used for bacteriacidal and thermoinsulatory purposes;

(3) indoles (indoles were observed in reptile Harderian glands by Vivien-Roels 1981); and (4) porphyrins. The Harderian gland actually contains, produces, and secretes porphyrins into the blood circulation (Payne 1994).

Fenestrated capillaries and sinusoids, both of which are indicative of an endocrine organ, have been found in Syrian hamster Harderian gland (Menendez-Pelaez et al. 1990), and various biochemical evidence for indole synthesis has been further reported (Menendez-

Pelaez et al. 1988a, b, and c).

In summary, if crocodilians do not have a epiphysis gland, then the major source of circulating melatonin needs to be identified. The Harderian gland is such a source in several tetrapod groups. Melatonin has a diverse number of functions, including immunological, regulation of the circadian rhythm, and regulation of the reproductive cycle. If the

Harderian gland is a primary melatonin source in crocodilians, then the gland may influence a multitude of important behaviors. The Harderian gland has a rich blood supply that is well connected with the brain supply and the blood supply to the retina, and salt gland. Studies in several amniotes have implicated autonomic innervation of the Harderian gland vasculature as the regulation of the gland and its secretion. Thus, the orbital vasculature may 349 provide the control of the Harderian gland and the major transport of its, potentially, biologically critical products. 350

LITERATURE CITED

Arad, Z. and Bernstein, M.H. 1988. Temperature regulation in turkey vultures. The Condor 90:913-919.

Arad, Z., Mitgard, U., and Bernstein, M.H. 1989. Thermoregulation in turkey vultures: vascular anatomy, arteriovenous heat exchange, and behavior. The Condor 91:505- 514.

Assenmacher, I. 1953. Etude anatomique du systeme arteriel cervico-cephalique chez l'oiseau. Archives d'Anatomie 35:181-202.

Baker, M. 1979. A brain cooling mechanism in mammals in vertebrates: physiology. W. H. Freeman and Co., San Francisco.

Bakker, R.T, Williams, M. & Currie, P. (1988). Nanotyrannus, a new genus of pygmy tyrannosaur, from the Latest Cretaceous of Montana. Hunteria 1:1-30.

Bamford, O.S. and Eccles, R. 1982. The central reciprocal control of nasal vasomotor oscillations. Pflügers Archiv. 394:139-143.

Bamford, O.S. and Eccles, R. 1983. The role of sympathetic efferent activity in the regulation of brain temperature. Pflügers Archiv. 396:138-143.

Bang, B.G. 1964. The nasal organs of the black and turkey vultures; a comparative study of the cathartid species Coragyps atratus atratus and Cathartes aura septentrionalis. Journal of Morphology 115:153-184.

Bang, B.G. 1971. Functional anatomy of the olfactory system in 23 orders of birds. Acta Anatomica 79:1-74.

351 Bang, B.G. and Wenzel, B.M. 1985. Nasal cavity and olfactory system; pp. 195-225 in A.S. King and J. McLelland (eds.), Form and Function in Birds, Vol. 3. Academic Press, London.

Baptiste, K.E. 1998. A preliminary study on the role of the equine guttural pouches in selective brain cooling. The Veterinary Journal 155:139-148.

Baptiste K.E., Naylor J.M., Bailey J., Barber E.M., Post K., & Thornhill J. 2000. A function for guttural pouches in the horse. Nature 403 : 382-383.

Baumel, J.J. 1967. The characteristic asymmetrical distribution of the posterior cerebral artery of birds. Acta Anatomica 67:53-59.

Baumel, J.J. 1975. Heart and blood vessels; pp. 1968-2009 in R. Getty (ed.), Sisson and Grossman’s The Anatomy of the Domestic Animals, 5th ed. Vol. 2. Saunders, Philadelphia.

Baumel, J.J. 1993. Systema Cardiovasculare; pp. 407-476 in J. J. Baumel (ed.), Handbook of Avian Anatomy: Nomina Anatomica Avium. Nuttall Ornithological Club, Cambridge, Mass.

Baumel, J.J, Dalley, A.F., and Quinn, T.H. 1983. The collar plexus of subcutaneous thermoregulatory veins in the Pigeon, Columba livia; its association with esophageal pulsation and gular flutter. Zoomorphology 102:215-239.

Baumel, J.J. and Witmer, L. M. 1993. Osteologia; pp. 45-132 in J. J. Baumel (ed.), Handbook of Avian Anatomy: Nomina Anatomica Avium. Nuttall Ornithological Club, Cambridge, Mass.

Bech, C. and Midtgard, U. 1981. Brain temperature and the rete mirable ophthalmicum in the zebra finch (Poephila guttata). Journal of Comparative Physiology B 145:89-93.

Beecher, W.J. 1951. A possible navigation sense in the ear of birds. American Midland Naturalist 46:367-384.

352 Beickert, P. 1951. Halbseitenrhythmus der vegetativen Innervation. Arch. Ohr.-, Nas.-u, Kehlk. Heilk. 157:404-41.

Bellairs, A.d’A and Kamal, A.M. 1981. The chondrocranium and the development of the skull in recent reptiles; pp. 1-263 in C. Gans and T.S. Parsons (eds.), Biology of the Reptilia, Vol. 11. Academic Press, New York.

Bellairs, A.d’A and Shute, C.C.D. 1953. Observations of the narial musculature of Crocodilia and its innervation from the sympathetic system. Journal of Anatomy 87:367-378.

Benton, M. J. 1999. Sclermochlus taylori and the origin of dinosaurs and pterosaurs. Philosophical Transactions of the Royal Society, London, Ser. B 354:1423-1446.

Benton, M. J. and Clarke, J.M. 1988. Archosaur phylogeny and the relationships of the Crocodylia; pp. 295-338 in The Phylogeny and Classification of the Tetrapods, vol. 1: Amphibians, Reptiles, Birds. Systematics Association Special Volume 35A. Clarendon Press, Oxford.

Bernstein, M., Duran, H., and Pinshow, B. 1984. Extrapulmonary gas exchange enhances brain oxygen in pigeons. Science 226:564-566.

Bojsen-Møller, F. and Fahrenkrug, J. 1971. Nasal swell-bodies and cyclic changes in the air passage of the rat and rabbit nose. Journal of Anatomy 110:25-37.

Brown, C.R. and Loveridge, J.P. 1981. The effect of temperature on oxygen consumption and evaporative water loss in Crocodylus niloticus. Comparative Biochemistry and Physiology 69A:51-57.

Bruner, H.L. 1907. On the cephalic veins and sinuses of reptiles, with description of a mechanism for raising the venous blood-pressure in the head. American Journal of Anatomy 7:1-117.

Bubien-Waluszewska, A. 1981. The cranial nerves; pp. 385-438 in A.S. King and J. McLelland (eds.), Form and Function in Birds, Vol. 2. Academic Press, London.

353 Bucana, C.D. and Nadakavukaren, M.J. 1972. Innervation of the hamster Harderian gland. Science 175:205-206.

Bugge, J. 1972. The cephalic arterial system in the insectivores and the primates with special reference to the Macroscelidoidea and Tupaioidea and the insectivore-primate boundary. Zoological Anatomy 135:279-300.

Bugge, J. 1974. The cephalic arterial system in insectivores, primates, rodents and lagomorphs, with special reference to the systematic classification. Acta Anatomica. 87: sppl. 62, pp. 1-160.

Bugge, J. 1979. Cephalic arterial pattern in New World edentates and Old World pangolins with special reference to their phylogenetic relationships and taxonomy. Acta Anatomica 105:37-046.

Burgoon, D.A., Kilgore Jr., D.L., and Motta, P.J. 1987. Brain temperature in the calliope hummingbird (Stella calliope): a species lacking a rete mirabile ophthalmicum. Journal of Comparative Physiology. 157:583-588.

Burns, R.B. 1976. Specific antibody production against a soluble antigen in the Harderian gland of the domestic fowl. Clinical and Experimental Immunology 26:371-374.

Burns, R.B. 1977. Possible route of antigen uptake by the Harderian gland of the domestic fowl. British Poultry Science 18:407-409.

Burns, R.B. and Maxwell, M.H. 1979. The structure of the Harderian and lacrimal gland ducts of the turkey, fowl and duck. A light microscope study. Journal of Anatomy 128:285-292.

Busbey, A.B. 1989. Form and function of the feeding apparatus of Alligator Mississippiensis. Journal of Morphology 202:99-127.

Butler, A.B. and Hodos, W. 1996. Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. Wiley-Liss, New York.

354 Cabanac, M. 1995. Human Selective Brain Cooling. R.G. Landes, Springer-Verlag, Austin.

Cauna, N. and Cauna, D. 1975. The fine structure and innervation of the cushion veins of the human nasal respiratory mucosa. Anatomical Record 181:1-16.

Chiasson, R.B. 1962. Laboratory Anatomy of the Alligator. W.M. C. Brown Company Pub, Debuque, Iowa.

Ching, A.T., Hughes, M.R., Poon, A.S., and Pang, S.F. 1999. Melatonin receptors and melatonin inhibition of duck salt gland secretion. General and Comparative Endocrinology 116:229-240.

Clarke, J.M., Welman, J., Gauthier, J.A., and Parrish, J.M. 1993. The laterosphenoid bone of early archosauriforms. Journal of Vertebrate Paleontology 13:48-57.

Cooper, A., Lalueza-Fox, C., Anderson, S., Rambaut, A., Austin, J., and Ward, R. 2001. Complete mitochondrial genome sequences of two extinct moas clarify Ratite evolution. Nature 409:704-707.

Coulombre, A.J., and Crelin, E.S. 1958. The role of the developing eye in the morphogenesis of the avian skull. American Journal of Physical Anthropology 16:25-37.

Cracraft, J. 2001. Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event. Proceedings of the Royal Society, London 268:459-469.

Cracraft, J. and Clarke, J. 2001. The basal clades of modern birds; pp. 143-156 in J. Gauthier, L.F. Gall, (eds.) New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom; 1999 Feb 12-14; Peabody Museum of Natural History, Yale University, New Haven, CT.

Craigie, E.H. 1941. Vascularization in the brains of reptiles. Transactions of the Royal Society of Canada 35:35-50.

355 Crawford, E.C., Jr., and Schmidt-Nielsen, K. 1967. Temperature regulation and evaporative cooling in the ostrich. American Journal of Physiology 212:347-353.

Cuthbertson, S., Jackson, B., Toledo, C., Fitzgerald, M.C., Shih, Y.F., Zagvazdin, Y., and Reiner, A. 1997. Innervation of orbital and choroidal blood vessels by the pterygopalatine ganglion in pigeons. The Journal of Comparative Neurology 386:422-442.

Dawes J.D. and Prichard M. 1953. Studies of vascular arrangements of nose. Journal of Anatomy 87:311-322.

De Beer, G.R. 1937. The Development of the Vertebrate Skull. Clarendon Press, Oxford.

Diefenbach, C.O. 1975. Thermal preferences and thermoregulation in Caiman crocodilus. Copeia 1975:530-540.

Djeridane, Y. 1994. Immunohistochemical evidence for the presence of vasopressin in the rat Harderian gland, retina and lacrimal gland. Experimental Eye Research 59:117- 120.

Døving, K.B. and Trotier, D. 1998. Structure and function of the vomeronasal system. Journal of Experimental Biology 201:2913-2925.

Dubey, S. and Haldar, C. 1997. Environmental factors and annual Harderian-epiphysis- gonadal interrelationship in indian jungle bush quail, Perdicula asiatica. General and Comparative Endocrinology 106:17-22.

Dyke, C.G., Davidoff, L.M. and Masson, C.B. 1933. Cerebral hemiatrophy with homolateral hypertrophy of the skull and sinuses. Surgery, Gynecology, and Obstetrics 57:588- 600.

Eccles, R. 1996. A role for the nasal cycle in respiratory defense. European Respiratory Journal 9:371-376.

Eccles, R. and Lee, R.L. 1981. Nasal vasomotor oscillations in the cat associated with the respiratory rhythm. Acta Otolaryngology 92:357-361. 356 Eccles, R. and Wallis, D.I. 1976. Characteristics of the sympathetic innervation of the nictitating membrane and of the vasculature of the nose and tongue of the cat. Journal of Neural Transmission 39:113-130.

Edgeworth, F.H. 1935. The Cranial Muscles of the Vertebrates. Cambridge University Press, London.

Elzanowski, A. 1987. Cranial and eyelid muscles and ligaments of the tinamous (Aves: Tinamiformes). Zoologische Jahrbücher Anatomie. 116:63-118.

Elzanowski, A. and Galton, P.M. 1991. Braincase of Enaliornis, an early cretaceous bird from England. Journal of Vertebrate Paleontology 11:90-107.

Evans, H.E. 1993. Miller’s Anatomy of the Dog, Fifth Edition. W.B. Saunders Company, London, Philadelphia.

Ferguson, M. 1981. The structure and development of the palate in Alligator mississippiensis. Archives of Oral Biology 26:427-443.

Ferguson, M. 1984. Craniofacial development in Alligator Mississippiensis; in M. Ferguson (ed.) The Structure, Development, and Evolution of Reptiles, Symposium Zoological Society of London 52:223-273.

Flanagan, P. and Eccles, R. 1997. Spontaneous changes of unilateral nasal airflow in man. A re-examination of the 'nasal cycle'. Acta Otolaryngology 117:590-595.

Fourman, J. and Ballantyne, B. 1967. Cholinesterase activity in the Harderian gland of Anas domesticus. The Anatomical Record 159: 17-028.

Frey, E. 1988. Das Tragsystem der Krokodile—eine biomechanische und phylogenetische Analyse. Stuttgarter Beiträge zur Naturkunde Serie A (Biologie) 426:1-60.

Ganey, T., Ogden, J. and Olsen, J. 1990. Development of the giraffe horn and its blood supply. The Anatomical Record 227:497-507.

357 Gauthier, J. 1986. Saurischian monophyly and the origin of birds; pp 1-55 in K. Padian (ed.). The Origin of Birds and the Evolution of Flight. San Francisco: California Academy of Sciences. (Memoirs of the California Academy of Sciences 8.).

Geisler, J.H. and Luo, Z. 1998. Relationships of Cetacea to terrestrial ungulates and the evolution of cranial vasculature in Cete; pp. 163-212 in J. Thewissen (ed.) The Emergence of Whales. Plenum Press, New York.

Gern, W.A. and Ralph, C.L. 1979. Melatonin synthesis by the retina. Science 204:183-184.

Ghoshal, N.G. 1985. Thermoregulatory role of the cranial circulation in cerebral temperature control. Vlaams Diergeneeskundig Tijdschrift 54 (4):246-261.

Goodman, D.C. and Fisher, H.I. 1962. Functional anatomy of the feeding apparatus in waterfowl (Aves: Anatidae.) Southern Illinois University Press, Carbondale.

Gower, D.J. and Walker, A.D. New data on the braincase of the aetosaurian archosaur. (Reptilia: Diapsida) Stagonolepis robertsoni Agassiz. in prep.

Grevers, G. 1989. Functional morphology of endonasal blood capillaries. Laryngology Rhinology Otology 68:23-8.

Grevers, G. 1993. The role of fenestrated vessels for the secretory process in the nasal mucosa: A histological and transmission electron microscopic study in the rabbit. Laryngoscope 103 (11):1255-1258.

Grevers, G. 1994. Electron-microscopic observations on the muscular coat of swell bodies in human nasal mucosa. Laryngoscope 104 (10):1285-1289.

Grevers, G. and Hermann, U. 1987. The “cavernous” tissue of the nasal mucosa. Laryngology Rhinology Otology 66:152-6.

358 Grevers, G. and Kamargakis, W. 1995. Intervascular smooth muscle fibers and muscular bolsters in nasal swell bodies of humans. Annals of Otology Rhinology and Laryngology 104:144-8.

Gupta, S.K. and Maiti, B.R. 1983. Influence of sex-hormones on the Harderian gland activity in female domestic duckling. Mikroskopie 40:132-137.

Gwinner, E. and Dittami, J. 1980. Epiphysisectomy affects the circannual testicular rhythm in European starlings (Sturnus vulgaris). Journal of Comparative Physiology 136:345- 348.

Hafferl, A. 1933. Gefasssystem. V. Das Ateriensystem; pp. 583-684 in L. Bolk, E. Goppert, E. Kalius, and W. Lubosc (eds.), Handbuch der vergleichenden Anatomie der Wirbeltiere, 6. Urban and Schwarzenberg, Berlin and Vienna.

Haldar, C, and Guchhait, P. 2000. Pineal gland of a nocturnal bird, Indian spotted owlet, Athene brama, morphological and endocrine observations. Journal of Experimental Zoology 287:145-150.

Hanken, J. 1983. Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia, Plethodontidae). II. The fate of the brain and sense organs and their role in skull morphogenesis and evolution. Journal of Morphology 177:255-268.

Hillenius, W.J., Watrobski, L.K., and Rehorek, S.J. 2001. Passage of tear duct fluids through the nasal cavity of frogs. Journal of Herpetology 35:701-704.

Hochstetter, F. 1906. Beitrage zur Anatomie und Entwickelungsgechichte des Blutgefassystemes der Krokodile. A. Voeltzkow (ed.). Reise in Ostafrika 4:1-139.

Hopson, J.A. 1979. Paleoneurology; pp. 39-146 in C. Gans, G. R. Northcutt, and P. Ulinski (eds.) Biology of the Reptilia, Vol. 9. Academic Press, New York.

359 Hossler, F.E. and Olson, K.R. 1984. Microvasculature of the avian eye: studies on the eye of the duckling with microcorrosion casting, scanning electron microscopy, and stereology. The American Journal of Anatomy 170:205-221.

Hughes, A.F.W. 1934. On the development of the blood vessels in the head of the chick. Philosophical Transactions of the Royal Society of London 224:75-129.

Iordansky, N.N. 1964. The jaw muscles of the crocodiles and some relating structures of the crocodilian skull. Anatomische Anzeiger 115:256-280.

Iordansky, N.N. 1973. The skull of the Crocodilia; pp. 201-262 in C. Gans and T.S. Parsons (eds.), Biology of the Reptilia, Vol. 4. Academic Press, New York.

Iordansky, N.N. 2000. Jaw muscles of the crocodiles: structure, synonymy, and some implications on homology and functions. Russian Journal of Herpetology 7:41-50.

Jessen, C. 1999. Brain cooling: an economy mode of temperature regulation in artiodactyls. News in Physiological Science 13:281-286.

Jollie, M. 1962. Chordate Morphology. Reinhold Publishing Corporation, New York.

Kaku, K. 1959. On the vascular supply in the brain of the domestic fowl. Fukuoka Acta Medica 50:4293-4306. Kavaliers, M. 1980. Extraretinal mediation of responses to temperature and light in hatchling alligators. Journal of Comparative Physiology 136:243-246.

Kavaliers, M, Ralph, CL. 1981. Encephalic photoreceptor involvement in the entrainment and control of circadian activity of young American alligators. Physiology and Behavior 26:413-418.

Kilgore, D., Bernstein, M., and Hudson, D. 1976. Brain temperatures in birds. Journal of Comparative Physiology B 1110:209-215.

360

Kilgore, D., Bernstein, M., and Schmidt-Nielsen, K. 1973. Brain temperature differences in a large bird, the rhea. American Journal of Physiology 225:739-742.

Kilgore, D., Boggs, D., and Birchard, G.F. 1979. Role of the rete mirable opthalmicum in maintaining the body-to-brain temperature difference in pigeons. Journal of Comparative Physiology 129:119-122.

Komárek, V. 1979. Anatomia Avium Domesticarum. Príroda, Vydavatel’stvo kníh a Casopisov, N.P. Bratislava.

Kumazaki T. 1991. Development of a new digital angiography system—improvement of rotational angiography and three dimensional image display. (In Japanese, English Abstract.) Nipp Acta Radiol 51:1068–1077.

Lakjer, T. 1926. Die Trigeminus-Versorgte Kaumuskulature der Sauropsiden. Auf kosten der Carlsbergstiftung, Kopenhagen.

Lang, J.W. 1976. Amphibious behavior of Alligator mississippiensis: roles of a circadian rhythm and light. Science 191:575-577.

Lasiewski, R.C. and Bartholomew, G.A. 1966. Evaporative cooling in the poor-will and tawny frogmouth. The Condor 68:253-262.

Livezey, B.C. 1997. A phylogenetic analysis of basal Anseriformes, the fossil Presbyornis, and the interordinal relationships of waterfowl. Zoological Journal of the Linnean Society 121(4):361-428.

Livezey, B.C. and Zusi, R.L. 2001. Higher-order phylogenetics of modern Aves based on comparative anatomy. Netherlands Journal of Zoology 51:179-205.

Lucas, A.M. and Stettenheim, P.R. 1972. Avian Anatomy—Integument. Agriculture Handbook 362. U.S. Government Printing Office, Washington, D. C.

361 Lunsford L.D., Maroon J.C., Bank W.O., Drayer B.P., and Rosenbaum A.E. 1977. Localization of velum interpositum AVM with metrizamide ventriculography and simultaneous stereoangiography. Journal of Neurosurgery 47:623–625.

Maklad, A., Quinn, T., and Fritzsch, B. 2001. Intracranial distribution of the sympathetic system in mice: DiI tracing and immunocytochemical labeling. The Anatomical Record 263:99-111.

McLelland, J. 1993. Apparatus Digestorius (systema alimentarium); in: Handbook of Avian Anatomy: Nomina Anatomica Avium, J.J. Baumel (ed.) Nuttall Ornithological Club, Cambridge, Mass.

Menendez-Pelaez, A., Reiter, R.J., Guerrero, J.M., Puig-Domingo, M., and Howkes, K.A. 1988a. Sexual dimorphism in N-acetyltransferase activity, Hydroxyindole-O- Methyltransferase activity and melatonin content in the Harderian glands of syrian hamsters: changes following gonadectomy. Proceedings of the Society for Experimental Biology and Medicine 187: 287-291.

Menendez-Pelaez, A., Reiter, R.J., Guerrero, J.M., Santana C., Howkes, K.A., and Gonzalez- Brito, A. 1988b. N-acetyltransferase activity and melatonin concentrations in the Harderian glands of female syrian hamsters : alterations following either epiphysisectomy or bilateral superior cervical ganglionectomy. Biochemical Archives 4: 231-238.

Menendez-Pelaez, A., Reiter, R.J., Howkes, K.A., Puig-Domingo, M., Vaughan, M.K., and Troiani, ME. 1988c. Harderian gland N-acetyltranferase activity in the male syrian hamster: effects of gonadectomy, short photoperiod exposure or subcutaneous melatonin implants. Endocrine Research 14: 121-130.

Menendez-Pelaez, A., Tolivia, D., Rodriguez-Colunga, M.J., and Reiter, R.J. 1990. Ultrastructure of the blood vessels in the Harderian gland of the hamster (Mesocricetus auratus): existence of sinusoids. Journal of Morphology. 204: 257-263.

Merck, J.W. 1997. A Phylogenetic Analysis of the Euryapsid Reptiles. Unpublished PhD. dissertation. University of Texas, Austin.

362 Mitgard, U. 1983. Scaling of the brain and the eye cooling system in birds: A morphometric analysis of the rete ophthalmicum. The Journal of Experimental Zoology 225:197- 207.

Mitgard, U. 1984a. Blood vessels and the occurrence of arteriovenous anastomoses in cephalic heat loss areas of mallards, Anas platyrhynchos, Aves. Zoomorphology 104:323-335.

Mitgard, U. 1984b. The blood vascular system in the head of the Herring Gull (Larus argentatus). Journal of Morphology 179:135-152.

Moss, M.L., 1971. Functional cranial analysis and the functional matrix. American Speech and Hearing Association Reports 6:5-18.

Moyer, R.W., Firth, B.T., and Kennaway, D.J. 1997. Effect of variable temperatures, darkness and light on the secretion of melatonin by epiphysis explants in the gecko, Christinus marmoratus. Brain Research 747:230-235.

Murakami, N., Kawano, T., Nakahara, K., Nasu, T., and Shiota, K. 2001. Effect of melatonin on circadian rhythm, locomotor activity, and body temperature in the intact house sparrow, Japanese quail and owl. Brain Research 889:220-224.

Negus, V. 1958. The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses. Livingstone, Edinburgh and London.

Ninomiya, H. and Nakamura, T. 1981. Vascular architecture of the canine prepuce. Zbl Veterinary Medicine C, Anatomy Histology Embryology 10:351-360.

Noden, D.M. 1983. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. American Journal of Anatomy 168:257-276.

Noden, D.M. 1986. Patterning of avian craniofacial muscles. Developmental Biology 116:347-356.

363 Norell, M.A., Clark, J.M., and Makovicky, P.J. 2001. Phylogenetic relationships among coelurosaurian theropods; pp. 49-67 in J. Gauthier, L.F. Gall, (eds.), New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom; 1999 Feb 12-14; New Haven, CT. Peabody Museum of Natural History, Yale University.

O’Donoghue C.H. 1921. The blood vascular system of the tuatara, Sphenodon punctatus. Transactions of the Royal Society of London 210(B):175–252.

Ostrom, J.H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnaean Society of London 8:91-182.

Owen, R. 1850. On the communications between the cavity of the tympanum and the palate in the Crocodilia (gavials, alligators and crocodiles). Philosophical Transactions of the Royal Society, London 1850:521-527.

Owen, R. 1866. On the Anatomy of the Vertebrates, Vol. 1: Fishes and Reptiles. Longmans, Green and Co., London.

Padian, K. and Chiappe, L.M. 1998. The early evolution of birds. Biological Review 73:1-42.

Papp, M.J., and Witmer, L. 1998. Cheeks, beaks, and freaks: a critical appraisal of buccal soft-tissue anatomy in ornithischian dinosaurs. Journal of Vertebrate Paleontology 18, (Supplement to 3) 76A.

Parker, W.K. 1866. On the structure and development of the skull in the ostrich tribe. Philosophical Transactions of the Royal Society of London 156:113-183.

Parker, W.K. 1869. On the structure and development of the skull of the common fowl (Gallus domesticus). Philosophical Transactions of the Royal Society of London 159:755-807.

Parrish, J. 1993. Phylogeny of the Crocodylotarsi, with reference to archosaurian and crurotarsan monophyly. Journal of Vertebrate Paleontology 13 (3):287-308.

Payne, A.P. 1994. The Harderian gland: a tercentennial review. Journal of Anatomy 185:1-49.

364

Pinshow, B., Bernstein, M., and Arad, Z. 1985. Effects of temperature and Pco2 on O2 affinity of pigeon blood: implications for brain O2 supply. American Journal of Physiology R758-R764.

Pinshow, B., Bernstein, M., Lopez, G., and Kleinhaus, S. 1982. Regulation of brain temperature in pigeons: effects of corneal convection. American Journal of Physiology 242: R578-R564.

Poe, S. 1997. Data set incongruence and the phylogeny of crocodilians. Systematic Biology 45:393-414.

Pohlman, A.G. 1921. The position and functional interpretation of the elastic ligaments in the middle-ear region of Gallus. Journal of Morphology 35:229-262.

Presley, R. 1993. Preconception of adult structural pattern in the analysis of the developing skull; pp. 347-377 in , J. Hanken and B. J. Hall (eds.), The Skull, Vol. 1. University Press, Chicago.

Principato, J. and Ozenberger, J. 1970. Cyclical changes in the nasal resistance. Archives of Otolaryngology 91:71-77.

Prum, R.O. 2002. Why ornithologists should care about the theropod origin of birds. The Auk 119:1-17.

Quay, W.B. 1979. The parietal eye – epiphysis complex; pp. 245-406 in C. Gans, R.G. Northcutt, and P. Ulinski (eds.), Biology of the Reptilia, Vol. 9. Academic Press, New York.

Rathke, M.H. 1866. Untersuchungen über die Entwickelung und den Körperbau der Krokodile. (W. von Wittich, ed.) F. Vieweg und Sohn, Braunschweig.

Reese, A.M. 1914. The vascular system of the Florida Alligator. Proceedings of the Academy of Natural Sciences of Philadelphia 66:413-425.

Reese, A.M. 1924. The cephalic glands of Alligator mississippiensis, Florida alligator, and of Agkistrodon, copperhead and moccasin. Biologia Generalis 1:482-499. 365 Rehorek, S.J. 1997. Squamate Harderian gland: an overview. The Anatomical Record 248:301-306.

Rehorek, S.J., Firth, B.T., and Hutchinson, M.N. 2000a. Can an orbital gland function in the Vomeronasal sense? A study of the pygopodid Harderian gland. Canadian Journal of Zoology 78:648-654.

Rehorek, S.J., Firth, B.T., and Hutchinson, M.N. 2000b. The structure of the nasal chemosensory system in squamate reptiles. I. The olfactory organ, with special reference to olfaction in geckos. Journal of Biosciences 25:173-179.

Rehorek, S.J., Firth, B.T., and Hutchinson, M.N. 2000c. The structure of the nasal chemosensory system in squamate reptiles. II. Lubricatory capacity of the vomeronasal organ. Journal of Biosciences 25:181-190.

Rehorek, S.J., Leigh, C.M., and Firth, B.T. 1999. Rate of protein synthesis of the Harderian gland of a skink, Hermiergis devresienses: a preliminary study. Copeia 2:526-528.

Richards, S.A. 1967. Anatomy of the arteries of the head in the domestic fowl. Journal of Zoology, London 152:221-234.

Richards, S.A. 1968. Anatomy of the veins of the head in the domestic fowl. Journal of Zoology, London 154:223-234.

Richards, S.A. 1970. Brain temperature and the cerebral circulation in the chicken. Brain Research 23:265-268.

Richardson, H. and Seebohm, P. 1968. Nasal airway response to exercise. Journal of Allergy 41:269-284. Ritter, F. 1970. The vasculature of the nose. Annals of Otology Rhinology and Laryngology 79:468-474.

Ross, A.T. 1941. Cerebral hemiatrophy with compensatory homolateral hypertrophy of the skull and sinuses, and diminuition of cranial volume. American Journal of Roentgenology 45:332-341.

366 Sampson, S.D. and Witmer, L.M. 1999. Novel narial anatomy in ceratopsid dinosaurs. Journal of Vertebrate Paleontology 19, (Supplement to 3).

Schumacher, G.H. 1973. The head muscles and hyolaryngeal skeleton of turtles and crocodilians; pp. 101-200 in C. Gans and T.S. Parsons (eds.), Biology of the Reptilia, Vol. 4. Academic Press, New York.

Schwenk, K. (ed.). 2000. Feeding: Form, Function and Evolutiion in Tetrapod Vertebrates. Academic Press, San Diego.

Sedlmayr, J.C. 2001. Encephalic blood vessels and the evolution of the braincase in archosaurs. Journal of Vertebrate Paleontology 21:100A.

Sedlmayr, J.C. and Witmer, L.M. 1998. Facial vasculature in extant Crocodylia with special reference to narial cavernous tissue. Journal of Vertebrate Paleontology 18, (Supplement to 3): 76A.

Sedlmayr, J.C. and Witmer, L.M. 1999. Cephalic vasculature in extant and fossil Archosauria, with special emphasis on the nasal region. Journal of Vertebrate Paleontology 19, (Supplement to 3).

Sereno, P.C. 1991. Basal archosaurs: phylogenetic relationships and functional implications. Society of Vertebrate Paleontology Memoir 2:1-53.

Sereno, P.C. 1999. The evolution of dinosaurs. Science 284:2137-2147.

Shiino, K. 1914. Das Chondrocranium von Crocodylus porosus mit Berucksichtigung der Gehirnnerven und Kopfgefasse. Anatomische Hefte 50:257-381.

Shindo, T. 1914. Zur vergleichenden anatomie der arteriellen kopffefaBe. Anatomische Hefte 1 (51):267-356.

Sibley, C.G. and Ahlquist, J.E. 1990. Phylogeny and Classification of Birds: A Study in Molecular Evolution. Yale University Proceedings, New Haven, CT.

367 Slonaker, J.R. 1918. A physiological study of the anatomy of the eye and its accessory parts of the English sparrow (Passer domesticus). Journal of Morphology 31:351-459.

Smith C.L.,and Smith G.R. 1967. A technique for making stereoscopic radiographs of animal skeletons. Copeia 4:848–850.

Spotila, J.R., Terpin, K., and Dodson, P. 1977. Mouth gaping as an effective thermoregulatory device in alligators. Nature 265:235-236.

Sudhakumari, C.C., Haldar, C., and Senthilkumaran, B. 2001. Seasonal changes in adrenal and gonadal activity in the quail, Perdicula asiatica: Involvement of the epiphysis gland. Comparative Biochemistry and Physiology 128B:793-804.

Tarsitano, S.F. 1985. Cranial metamorphosis and the origin of the Eusuchia. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 170:27-44.

Tatum, A. 1923. The effect of deficient and excessive pulmonary ventilation on nasal volume. American Journal of Physiology 42:175-179.

Tompsett DH. 1970. Anatomical techniques. 2nd ed. Livingstone, London.

Underwood, G. 1970. The eye; pp. 1-93 in C. Gans (ed.), Biology of the Reptilia, Vol. 2. Academic Press, New York.

Vakkuri, O., Rintamaki, H., and Leppaluoto, J. 1985. Presence of immunoreactive melatonin in different tissues of the Pigeon (Columba livia). General and Comparative Endocrinology 58:69-75.

Vanden Berge, J. and Zweers, G. 1993. Myologia; pp. 189-250 in , J. J. Baumel (ed.), Handbook of Avian Anatomy: Nomina Anatomica Avium. Nuttall Ornithological Club, Cambridge, Mass.

Vilchis, F., Chavez, B., and Perez-Palacios, G. 1991. Steroid hormone binding in the Harderian gland of birds: characteristics of the androgen, estrogen, and progestin receptors of Anas platyrhynchos and Gallas domesticus. General and Comparative Endocrinology 82:425-433.

368 Walls, G.L. 1942. The Vertebrate Eye and Its Adaptive Radiation. The Cranbrook Press, Bloomfield Hills, Michigan.

Wasicko, M.J., Hutt, D.A., Parisi, R.A., Neubauer, J.A., Mezrich, R., and Edelman, N.A. 1990. The role of vascular tone in the control of upper airway collapsibility. American Review of Respiratory Disease 141:1569-1577.

Watanabe, T. and Yasuda, M. 1968. Peripheral course of the olfactory nerve in the fowl. Japanese Journal of Veterinary Science 30:275-279.

Welman, J. 1995. The Evolution of the Braincase of Early Diapsids and its Bearing on the Origin of Dinosaurs, Crocodiles and Birds. Unpublished PhD. dissertation. University of the Orange Free State.

Wetterberg, L., Yuwiler, A., Geller, E., and Shapiro, S. 1970a. Harderian gland: development and influence of early hormonal treatment on prophyrin content. Science 168:996- 998.

Wetterberg, L., Yuwiler, A., Ulrich, R., Geller, E., and Wallace, R. 1970b. Harderian gland: influence on epiphysis Hydroxyindole-O-Methyltransferase activity in neonatal rats. Science 170:194-196.

Wharton, D.S. 2000. An enlarged endocranial venous system in Steneosaurus pictaviensis (Crocodylia: Thalattosuchia) from the Upper Jurassic of Les Lourdines, France. Comptes Rendus de l'Academie des Sciences Series IIA Earth and Planetary Science 331(3):221-226.

Wharton, D.S. and Sedlmayr, J.C. 2000. A new look at the archosaurian cranial venous system, with special emphasis on endocephalic drainage. Journal of Vertebrate Paleontology 20:78A.

Wible, J.R. 1984. The Ontogeny and Phylogeny of the Mammalian Cranial Arterial Pattern (Internal Carotid Artery). Unpublished PhD.dissertation. Duke University, Durham.

Wible, J.R. 1986. Transformation in the extracranial course of the internal carotid artery in mammalian phylogeny. Journal of Vertebrate Paleontology 6:313-325.

369 Wible, J.R. 1987. The eutharian stapedial artery: character analysis and implications for superordinal relationships. Zoological Journal of the Linnean Society 91107-135.

Wible, J.R. and Hopson, J.A. 1995. Homologies of the prootic canal in mammals and non- mammalian cynodonts. Journal of Vertebrate Paleontology 15:331-356.

Wible, J.R. and Zeller, U. 1994. Cranial circulation of the pen-tailed tree shrew Ptilocercus lowii and relationships of Scandentia. Journal of Mammalian Evolution 2:209-230.

Wingstrand, K.G. 1951. The structure and development of the avian hypophysis. C.W.K. Gleerup, Lund.

Witmer, L.M. 1990. The craniofacial air sac system of Mesozoic birds (Aves). Zoological Journal of the Linnean Society 100:327-378.

Witmer, L.M. 1992. Ontogeny, Phylogeny, and Air Sacs: The Importance of Soft-Tissue Inferences in the Interpretation of Facial Evolution in Archosauria. Unpublished PhD Dissertation. John Hopkins University School of Medicine, Baltimore.

Witmer, L.M. 1995a. The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils. pp.19-33 in: Functional Morphology in Vertebrate Paleontology, J. J. Thomason (ed.), Cambridge University Press, New York.

Witmer, L.M. 1995b. Homology of facial structures in extant archosaurs (birds and crocodilians), with special reference to paranasal pneumaticity and nasal conchae. Journal of Morphology 225:269-327.

Witmer, L.M. 1997. The evolution of the antorbital cavity of archosaurs: a study in soft- tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. Memoirs of the Society of Vertebrate Paleontology, Journal of Paleontology 17(Supplement to 3):1-73.

Witmer, L.M. 1998. Applications of the extant phylogenetic bracket (EPB) approach to the problem of anatomical novelty in the fossil record. Journal of Vertebrate Paleontology 18, (Supplement to 3): 76A. 370 Witmer, L.M. 2001. Nostril position in dinosaurs and other vertebrates and its significance for nasal function. Science 293:749-1000.

Witmer, L.M. and Sampson, S.D. 1999. Nasal conchae and blood supply in some dinosaurs: physiological implications. Journal of Vertebrate Paleontology 19:85A.

Witmer, L.M. and Sampson, S.D. in prep. Case studies in novel narial anatomy II: the Gharial. Wu X.-C. and Chatterjee, S. 1993. Dibrothosuchus elaphros, a crocodylomorph from the Lower Jurassic of China and the phylogeny of the Sphenosuchia. Journal of Vertebrate Paleontology 13:85-89.

Young, R.W. 1959. The influence of cranial contents on postnatal growth of the skull in the rat. American Journal of Anatomy 105:383-415.

Zangerl R. 1965. Radiographic techniques in Kummel B, Raup DM, (eds.) Handbook of Paleontological Techniques. San Francisco: Freeman. p 305–320.

Zangerl R, and Schultze H-P. 1989. X-radiographic techniques and applications; pp. 165- 177. in Feldman R.M., Chapman R., Hannibal J.T., (eds.). Paleotechniques. Lawrence: Paleontological Society, Special Publication 4.

Zusi, R.L. 1983. Patterns of diversity in the avian skull; pp. 391-437 in J. Hanken and B.K. Hall (eds.), The Skull. Vol. 2. The University of Chicago Press, Chicago and London.

Zusi, R.L. and Storer, R.W. 1969. Osteology and mycology of the head and neck of the pied- billed grebes (Pobilymbus). Miscellaneous Publications of the Museum of Zoology, University of Michigan 139:1-49. 371 Table 1. Synonymy and skeletal attachments of craniocervical musculature (based on Sedlmayr and Holliday, in prep.).

Muscle (NAA) Crocodilian synonym Origin Insertion Complexus Spinalis capitis Chiasson Aves: Aves: 1962 lateral tubercles of transverse Occipital crest Transversospinalis processes Zusi and Storer 1969 Frey 1988 Crocodylia: transverse Crocodylia: processes roughened dorsomedial area of squamosal-crista occipitalis; supraoccipital Chiasson 1962

Biventer cervicis rectus capitis sublimis Aves: Aves: Chiasson 1962 caudal cervical spinous midline occipital crest; Transversospinalis cervicis processes horizontal transverse nuchal 1 crest ventral to m. Frey 1988 Crocodylia: complexus-between mm. cranial spinous processes, complexus and splenius more caudal than m. splenius capitis capitis Crocodylia: fossa on paraoccipital process; knobbed area on dorsolateral supraorbital; dorsolateral paraoccipital process, roughened area of supraoccipital, between mm. complexus and splenius capitis Chiasson 1962

Splenius capitis Rectus capitis profundus Aves: Aves: Chiasson 1962 spinous processes C-2, 3 caudal opisthotic process Obliquus capitis (paraocipital) deep to mm. Bakker et al 1988 Crocodylia: biventer and complexus; caudal and cranial spinous vertical transverse nuchal process, inserts into nuchal crest; medial to m. rectus crest capitis lateralis; rostral occiput

Crocodylia: dorsolateral paraoccipital process; occipital, deep to m. complexus Chiasson 1962

372 Table 1: continued Muscle (NAA) Crocodilian synonym Origin Insertion Splenius capitis Rectus capitis Aves: Aves: profundus spinous processes C-2, caudal opisthotic Chiasson 1962 3 process (paraocipital) Obliquus capitis deep to mm. biventer Bakker et al 1988 Crocodylia: and complexus; caudal and cranial vertical transverse spinous processes, nuchal inserts into nuchal crest crest; medial to m. rectus capitis lateralis; rostral occiput

Crocodylia: dorsolateral paraoccipital process; occipital, deep to m. complexus Chiasson 1962

Rectus capitis Trachleo-mastoideous Aves: Aves: lateralis Owen 1866 cranial transverse processes: Paraoccipital process and Collo-occipitalis lateral hypapophyses, vertical crest; Chiasson 1962 caudolateral crista dorsal occipital crest; Transversarius ventrolateralis paraoccipital process deep Bakker et 1988 and caudal to mm. Longus capitis profundus Crocodylia: depressor mandibulae and Frey 1988 lateral most transverse splenius capitis processes, cervical processes, and lateral hypapophyses Crocodylia: ventrolateral paraoccipital process; medial to foramen magnum on paraoccipital process; exoccipital and basioccipital Chiasson 1962

Rectus capitis Longissimus capitis Aves: Aves: dorsalis Chiasson 1963 medial ribs: cranial articular knob of basitemporal plate, Longus capitis superficialis processes and costal processes lateral to occipital condlyle; Frey 1988 caudolateral basal crest on Crocodylia: caudal basitemporal plate dorsal aspect of cervical articular processes Crocodylia: median basioccipital, more medial to m. rectus capitis ventralis; dorsal head to exocciptial, ventral head to basioccipital

373 Table 1: continued Muscle (NAA) Crocodilian synonym Origin Insertion Rectus capitis Collo-capitis Aves: Aves: ventralis Chiasson 1962 craniomedial hypapophyses, fleshy and median on Longus colli caudomedial pars lateralis of basioccipital; (rectus capitis costo- crista ventrolateralis/ crista on basitemporal plate vertebralis) crista ventralis corporis rostral to m rectus capitis Frey 1988 (median ventral crests on dorsalis; cranial and caudal cervical triangular area of vertebrae) basisphenoid rostral to bulla basitemporalis Crocodylia: median crista ventralis corporis Crocodylia: basal tubera, ventrolateral projecting aspects of basioccipital, very roughened 374 Table 2. Synonymy and skull attachments of archosaur jaw adductor musculature (Holliday and Sedlmayr, in prep.). *Rows of attachments divided into crocodilians on top and birds on bottom.

Crocodilian Synonym used Avian synonyms Origin* Insertion* synonyms

Rostroventrolateral quadrate, Lakjer (1926) and Lakjer (1926): m. Dorsal caudoventromedial Schumacher (1973): AME profundus; surangular rostral postorbital, and some M. AME pars Vanden berge and to articular fossa of dorsoventromedial superficialis and Zweers (1993): m. m. AME superficialis postorbital, attaching pars medialis; AME pars profunda to adductor tubercle Iordansky (2000): [caudalis]; Livezey and Caudodorsal face M. AME Zusi (2000): m. AME Laterorostral otic of the mandible superificialis articularis internus process of quadrate just rostral to attaching to adductor articular fossa tubercle

Fossa of otic process Lakjer (1926): m. AM lateral to trigeminal Mediodorsal Lakjer (1926): M. posterior; Elzanowski foramen attaching to surangular AME pars medialis (1987): m. AM adductor tubercle and and M. AME posterior; Vanden medialis crest m. AME medialis profundus part c. berge and Zweers Iordansky (1964) (1993): m. AM ossis Caudolateral face and Schumacher quadrati [caudalis]; Body of quadrate of mandible (1973): M. AME Livezey and Zusi between otic and caudal to lateral medialis. (2000): m. AM orbital processes and mandibular posterior attaches to tubercle of process when lateral orbital process present

Coronoid Lakjer (1926): m. rugosity, Lakjer (1926): m. AME profundus pars Within supratemporal rostromedial AME profundus caudalis and medialis; fenestra on parietal, cartilago pars anterior and Elzanowski (1987): squamosal and transiliens, and in middle. m. AME pars quadrate rostral internal Iordansky (2000): superficialis and m. m. AME profundus mandibular m. AME AME pars profunda; pars rostralis fenestra profundus; Vanden berge and

Schumacher (1973): Zweers (1993): m. Lateral mandible m. AME pars ventralis; rostral to pseudotemporalis Livezey and Zusi In fossa articularis, insertion of (part) (2000): m. AME medial to and on quadrate muscles articularis externus zygomatic process and lateral and zygomatica mandibular

process

375 Table 2: continued Crocodilian Synonym used Avian synonyms Origin* Insertion* synonyms

Lakjer (1926): m. On rostrodorsolateral AME profundus pars laterosphenoid between Dorsal cartilago rostralis and m. AME cotylar crest and dorsal transiliens superficialis; temporal fenestra dorsal Elzanowski (1987): to maxillary nerve canal m. pseudotemporalis m. AME (temporal part); profundus Vanden berge and pars caudalis Zweers (1993): m. Fossa coronoideus as Rostrolateral AME pars rostralis medial part of muscles mandible, (temporalis); attaching from fossa lateral, medial, Livezey and Zusi temporalis and/or region and/or directly (2000): m. AME between zygomatic and to coronoid coronoideus and postorbital process. process superficialis

Pseudotemporalis crest Caudodorsomedi on rostrolateral Lakjer (1926): m. al cartilago Lakjer (1926): m. laterosphenoid ventral to pseudotemporalis transiliens AME profundus pars maxillary nerve canal superficialis (part); anterior and m. Elzanowski (1987): m. pseudotemporalis. m. Pseudotempora- Iordansky (1964): m. Pseudotemporal quadratomandibularis lis pseudotemporalis and tubercle on (laterosphenoid part); Rostrolateral intermedius; medial mandible Vanden berge and laterosphenoid, medial to Schumacher (1973) or dorsorostral Zweers (1993): m. postorbital process, and Iordansky (2000): to medial pseudotemporalis ventral to circumorbital m. pseudotermporalis mandibular fossa superficialis ligament as far rostral

coronoid process

Caudal internal Caudolateral face of mandibular fossa pterygoid process of attatching along Lakjer (1926): M. Lakjer (1926): quadrate attaching to rostral articular AME profundus pseudotemporalis lateral and medial dorsal medial posteror portion (c) profundus; quadrate crests and and lateral and m. AME Elzanowski (1987): adductor tubercle borders of the posteror; m. angular Iordansky (1964): m. quadratomandibularis m. AM Caudalis AM posterior; (quadrate part); Caudomedial Schumacher (1973) Vanden berge and Rim and fossa of orbital mandible rostral M. AME medialis Zweers (1993): m. process of quadrate to medial (part), pars pseudotemporalis mandibular fossa profundus, and profundus or Mam posterior caudalis

376 Table 2: continued Crocodilian Synonym used Avian synonyms Origin* Insertion* synonyms Dorsal palatine, Caudomedial

pterygoid, caudodorsal articular and Lakjer (1926): m. maxilla, ventrolateral angular on pterygoideus dorsalis lacrimal and interorbital retroarticular pars lateralis and Lakjer (1926): septum process medialis; pterygoideus dorsalis; Elzanowski (1987): m. pterygoideus Iordansky (1964) and Medial m. pterygoideus pars dorsalis Schumacher (1973): mandibular fossa medialis dorsalis and m. pterygoideus on caudomedial pars lateralis dorsalis; anterior Dorsolateral palatine and mandible and in Vanden berge and pterygoid rostral fossa of Zweers (1993): m. medial pterygoideus pars mandibular dorsalis process

Lateral and Caudal rim of pterygoid Lakjer (1926): m. ventral angular and dorsomedial process pterygoideus ventralis on retroarticular of pterygoid pars lateralis and process Lakjer (1926): m. medialis; pterygoideus pars A- Elzanowski (1987): C; m. pterygoideus pars M pterygoideus Iordansky (1964) and medialis ventralis, Rostral rim and ventralis Schumacher (1973): Ventral palatine along pars rostralis, and medial tip of m. pterygoideus medial and lateral laminae pars caudalis; medial posterior choanalis and Vanden berge and mandibular medioventral pterygoid Zweers (1993): m. process pterygoideus pars ventralis

377 Table 3. Osteological correlates of encephalic vessels.

Vessel Osteological correlate Abducens vein Internal abducens foramen Cavernous sinus Walls of hypophyseal fossa Cerebellar auricular Cerebellar auricular sinus sinus foramen Cerebral carotid vein Cerebral carotid foramen and canal External occipital External occipital vein foramen Foramen magnum Foramen magnum sinus Marginal sinus Marginal crest Occipital sinus Fossa in ventral supraoccipital Oculomotor vein Internal oculomotor foramen Rostal semicircular Canal for rostral sinus semicircular sinus Sinus of basicranial Basicranial fenestra fenestra Sinus olfactorius Olfactory canal, foramen, and groove Sphenotemporal Tentorial crest sinus Superior sagittal Frontal crest sinus Torcular herophili Intersection of frontal and marginal crests Transverse sinus Marginal crest Trigeminal vein Internal trigeminal foramen Trochlear sinus Internal trochlear foramen Vagal sinus Groove leading into dorsal aspect metotic tissue

378 Table 4. Osteological correlates of the stapedial arterial system

Artery Osteological correlates Stapedial a Stapedial foramen Temporoorbital a Stapedial groove Temporoorbital canal Cranialquadrate canal Supraorbital a Supraorbital groove Ophthalmotemporal Cotylar crest External occipital a External occipital canal

379

381

Figure 2. Scatter plots of densitometer value versus the percent of barium in the injection medium for (A) common carotid, (B) palatine, (C) rhamphothecal, and (D) premaxillary arteries for nineteen duck heads injected with a barium/latex solution varying in 5% increments. Densitometer values are unit- less and are based on a scale of increasingly more darkly shaded bars numbered 1 to 21, with 1 being most radiodense (white; densitometer value of 0.0) and 21 most radiolucent (black; densitometer value of 3.24). Thus, the closer a reading is to 0.0, the more likely a vessel is to be visualized. The plots for the common carotid (A) and premaxillary (D) arteries illustrate an increase in vessel radiopacity with increasing barium content in the injection media; non-parametric Spearman rank correlation tests demonstrated a positively significant relationship between radiopacity and barium percentage (common carotid artery, Rho = 0.700; premaxillary artery, Rho = 0.730). The plots for the palatine (B) and rhamphothecal (C) arteries do not show statistically significant relationships (rhamphothecal artery, Rho = 0.18; palatine artery, Rho = 0.200). 382

Figure 3. Scatter plot illustrating the relationship between the number of vessels counted (with 20 total possible vessels) versus percent barium for 19 different vascular injection solutions. The graph illustrates a fairly constant number of observable vessels (between 16 and 19 vessels) in solutions with 20%–95% barium. However, a dramatic threshold occurs at 10% barium where the number of observable vessels decreases (four vessels at 10% barium, two vessels at 5% barium). Between 40% and 55% barium, vessel number counts decrease slightly, the result of extreme vessel profusion, as some vessels are lost from view within a dense tangle of vessels (i.e., retia and erectile tissues). The Spearman rank correlation tests did not find a significant relationship (Rho = 0.400). 383

Figure 4. Phylogenetic relationships of (A) Avemetatarsalia (topology based on Sereno 1991; Benton 1999; Merck 1997), (B) Crurotarsi (based on Sereno 1991; Parrish 1993; Gower and Walker in prep.), (C) Archosauromorpha (based on Gauthier 1986; Sereno 1991; Parrish 1993; Merck 1997).

384

Figure 5. Phylogenetic relationships of the extant avian taxa studied (topology after Sibley and Ahlquist 1990; Cooper et al. 2001; Cracraft 2001; Cracraft and Clarke 2001; Livezey and Zusi 2001). * denotes taxa studied by dissection.

385

Figure 6. Anas platyrhynchos. The major cephalic arteries and their relation to the bony skull in (A) lateral; (B) Dorsal; and (C) palatal views. Skull drawings based on Komárek (1979) and specimens. 386 Figure 6: B

387 Figure 6: C

C 388

Figure 7. Aquila chrysaetos. Schematic illustration of the antorbital sinus and the suborbital diverticulum during (A) jaw abduction and (B) jaw adduction. The curved arrow indicates the course of the airstream. Modified from Witmer (1995b).

389

Figure 8. Dendogram of the Nasal vestibular Vascular Plexus (NVVP) and its elements in extant Diapsida.

390

Figure 9. Phylogenetic relationships of Crocodylomorpha (topology based on Benton and Clarke 1988; Poe 1997; Brochu 1999). * denotes taxa studied by dissection. 391

Figure 10. Alligator mississippiensis. The major cephalic arteries and their relation to the bony skull in (A) right lateral, (B) dorsal, (C) palatal, and (D) occipital views. Skull drawings based on Jollie (1962) and specimens. 392 Figure 10: B

B 393

Figure 10: C

C 394

Figure 10: D

D 395

A Figure 11. Crocodylus novaeguineae. Juvenile. Medial view of right side in sagittal section depicting (A) the bony endocranium and (B) the cephalic arterial system. Rostral is toward the left of the page and dorsal toward the top. 396

Figure 11: B

B 397

geniohyoideous BIRDS

genioglossus

A geniohyoid pars rostralis hyoglossus primordium pars caudalis (external) sternohyoid rectus cervicis (tracheo-laryngo- hyoid) sternotrachealis cricohyoid (thyrohyoid) tracheohyoideous

(internal) cleidohyoid (omohyoid)

Figure 12. Diagrams of the major components and divisions of the hyobranchial musculature in (A) Aves and (B) Crocodylia, based on Edgeworth (1935). Terminology of avian muscles based on Vanden Berge and Zweers (1993). Parenthetical terms in (B) refer to term used by Schumacher (1973). 398 Figure 12: B

CROCODILES

B genioglossus geniohyoideous (includes branchiomandibular is spinalis) hypoglossus primordium inner: pars medialis (episternobranchialis) (external) rectus cervicis sternohyoid outer: pars lateralis joins geniohyoid by sternomandibularis tendon w/genioglossus (episternotendineous)

(internal) omohyoid (coracohyoid)